Final Study Report

OCS Study BOEMRE 2010-05

Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

Final Technical Summary Final Study Report

U.S. Department of the Interior BOEMRE Bureau of Ocean Energy Management, Regulation and Enforcement Pacific OCS Region

OCS Study BOEMRE 2010-05

Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

Final Technical Summary Final Study Report

Project Manager Peter T. Raimondi

Principal Investigators Richard Ambrose Jack Engle Steve Murray Jayson Smith

Study design, oversight, and funding were provided by the U.S. Department of the Interior, Bureau of Ocean Energy Management, Regulation and Enforcement, Environmental Studies Program, Washington, DC under Agreement Number M07AC12503 by

Center for Ocean Health Long Marine Laboratory University of California Santa Cruz, CA 93106

Disclaimer

This report has been reviewed by the Pacific Outer Continental Shelf Region, Bureau of Ocean Energy Management, Regulation and Enforcement, U.S. Department of the Interior and approved for publication. The opinions, findings, conclusions, and recommendations in this report are those of the authors, and do not necessarily reflect the views and policies of the Bureau of Ocean Energy Management, Regulation and Enforcement. Mention of trade names or commercial products does not constitute an endorsement or recommendation for use. This report has not been edited for conformity with Bureau of Ocean Energy Management, Regulation and Enforcement editorial standards.

Availability of Report Extra copies of the report may be obtained from:

U.S. Dept. of the Interior Bureau of Ocean Energy Management, Regulation and Enforcement Pacific OCS Region 770 Paseo Camarillo Camarillo, CA 93010 Phone: 805-389-7621

Suggested Citation

The suggested citation for this report is:

Raimondi, P.T. and R.N. Gaddam. Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007- 2010). BOEMRE OCS Study 2010-005. Center for Ocean Health, Long Marine Laboratory, University of California, Santa Cruz, California. BOEMRE Cooperative Agreement Number M07AC12503. 38 pages (plus appendix).

PROJECT ORGANIZATION Project Technical Officer:

Mary Elaine Helix, Bureau of Ocean Energy Management, Regulation and Enforcement (BOEMRE)

Report Authors:

Peter T. Raimondi, University of California, Santa Cruz Rani N. Gaddam, University of California, Santa Cruz

Key Project Personnel:

Principal Investigators: Peter T. Raimondi Richard F. Ambrose John M. Engle Steven N. Murray Jayson R. Smith

Project Staff: Stevie Adams Karah Ammann Laura Anderson Christy Bell Sean Bergquist Lisa Gilbane Galen Holt Steven Lee Dan Martin Melissa Miner Carla Navarro Melissa Redfield Rafe Sagarin Sean Vogt Stephen Whitaker

Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

TABLE OF CONTENTS PROJECT ORGANIZATION ...... 4 LIST OF FIGURES...... 2 LIST OF TABLES ...... 2 FINAL TECHNICAL SUMMARY ...... 3 FINAL STUDY REPORT...... 7 PART I: INTRODUCTION, OBJECTIVES, AND APPROACH...... 7 1.1 Introduction...... 7 Central and Southern California Rocky Intertidal Habitats ...... 8 San Luis Obispo and Northern Santa Barbara Counties (north of Point Conception) ...... 9 Southern Santa Barbara, Ventura, Los Angeles and Orange Counties (south of Pt. Conception) ...... 10 1.2 Objectives ...... 10 1.3 Approach...... 10 Target Species Monitoring...... 10 Coordination—Internal and with MARINe ...... 16 Data management...... 17 Project management...... 17 1.4 Significant Conclusions ...... 18 1.5 Study Results ...... 18 1.6 Study Product(s) ...... 18 Presentations (2007-2010) ...... 19 Publications (2007-2010)...... 26 Reports (2007-2010) ...... 28 Sample Data Requests (2010) ...... 30 ACKNOWLEDGEMENTS ...... 31 LITERATURE CITED ...... 32 APPENDIX ...... 34 Selected Publications (attached) ...... 34

1 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

LIST OF FIGURES Figure 1: Location of Sampling Sites ...... 12

LIST OF TABLES Table 1: Extent of rocky and sandy shores for central/southern California. (Mainland data from Littler and Littler, 1979. Island data from Littler and Littler 1980)...... 8 Table 2: Sites sampled from north to south, group and Principle Investigator (PI) responsible for sampling and the seasons that were sampled during the contractual period...... 11 Table 3: Target species sampled (X) at each of the 24 sample sites...... 14 Table 4: Target species plots in which motile organisms were sampled...... 15

2 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

FINAL TECHNICAL SUMMARY

STUDY TITLE: “Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities”

REPORT TITLE: Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities - Final report (2007-2010)”

CONTRACT NUMBER: Cooperative Agreement Number M07AC12503

SPONSORING OCS REGION: Pacific

APPLICABLE PLANNING AREA(S): Southern California

FISCAL YEAR(S) OF PROJECT FUNDING: FY 2007- FY2010

COMPLETION DATE OF REPORT: December 31, 2010

COSTS: FY2007 $325,237; FY 2008 $305,849; FY 2009 $320,414

PROJECT MANAGER(S): Dr. Peter Raimondi

AFFILIATION: Long Marine Laboratory, University of California, Santa Cruz (UCSC)

ADDRESS: UC Santa Cruz Office of Sponsored Projects, 1156 High Street, Santa Cruz, California

PRINCIPAL INVESTIGATOR(S): Dr. Pete Raimondi, University of California, Santa Cruz (UCSC); Dr. Richard Ambrose, University of California, Los Angeles (UCLA); Dr. Jack Engle, University of California, Santa Barbara (UCSB); Dr. Steve Murray, California State University, Fullerton (CSUF); Dr. Jayson Smith, California State University, Fullerton (CSUF)

KEY WORDS: rocky intertidal, monitoring, black abalone,

BACKGROUND

Oil and gas activities, especially the tankering of oil along the California coast and the extraction of oil from OCS activities, raise the possibility of an oil spill or other impact to coastal resources. Population monitoring of coastal biota in central and southern California provide baseline information in case an event such as a spill damaged these resources. BOEMRE initiated the formation of a long-term monitoring program, the Multi-Agency Rocky Intertidal Network, MARINe, in 1997, which now has 32 Federal, State and local agency, University and private partners and monitors 120 rocky shore

3 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

sites. Through this study, BOEMRE funds biannual monitoring at 24 established rocky intertidal sites along the California mainland adjacent to OCS operations. The study also funds operation and maintenance of the shared MARINe database, and coordination of the MARINe committees.

OBJECTIVES

The primary objective for this research is to contribute to the ongoing monitoring program that provides a basis for determining if change in rocky shoreline communities adjacent to producing OCS facilities can be attributed to producing operations or accidents from OCS facilities. The second objective is to provide an ecological context through monitoring so as to understand the natural and anthropogenic changes to these communities that have occurred in the Southern California Bight since the OCS program was initiated. This latter objective is based on a collaboration between MARINe and other groups (especially the Partnership for Interdisciplinary Study of Coastal Oceans (PISCO)) and includes the collection of additional biodiversity data and comparison to comparable historic data (using matching funds). Additional objectives included oversight of a concurrent database process and publication of metadata for the BOEMRE- funded long-term data set.

DESCRIPTION:

The work completed in the period 2007-2010 employed methodologies consistent with the previous MARINe projects in order to maximize comparability among project results. The methodological details for these projects can be found in Engle (2005 and www.marine.gov), and are summarized below.

To accomplish the first objective, target species at 24 established rocky intertidal sites along the mainland coast of Southern and Central California adjacent to producing platforms were monitored spring and fall.

Target species include: mussels (Mytilus californianus), barnacles (Chthamalus spp., Balanus glandula and Pollicipes polymerus), anemones (Anthopleura elegantissima), algal species including Endocladia muricata, Hesperophycus harveyanus, Silvetia compressa, Mazzaella spp., Mastocarpus papillatus, surfgrass (Phyllospadix scouleri/torreyi), motile invertebrates such as owl limpets (Lottia gigantea), black abalone (Haliotis cracherodii) and sea stars (Pisaster ochraceus). Mussels, barnacles, anenomes and algal species were photographed in fixed rectangular plots and scored in the lab or field (barnacles at some sites) by scoring species under 100 points on each slide. Five replicate plots per target species were photographed at each site where the plots occurred. Surfgrass cover was estimated using a point contact method along 10 m transects. Owl limpets were measured and counted in 5 replicate, 1-meter circular plots at each site where the plots occurred. Abalone were counted and measured in 3 replicate irregular plots. Sea stars were counted, measured and classed by color in either 2 meter wide, 10 m long band transects or irregular plots, depending on the habitat. In many of the target species plots we also sampled the associated motile species. To optimize future

4 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010) environmental impact assessments, sites have been established systematically over a broad geographic range and each species is monitored at several sites within that range. This study also included overall coordination of MARINe, including facilitating meetings with the MARINe Steering Committee, Data Panel, and Science Panel and coordinating use of the data in collaborative projects. A large MARINe database is also populated and maintained for the entire network through this Cooperative Agreement.

Dr. Pete Raimondi, the Project Manager, coordinated the study, and specifically oversaw monitoring in San Luis Obispo and northern Santa Barbara County sites. Dr. Steve Murray and Dr. Jayson Smith at California State University, Fullerton conducted the monitoring in Orange County. Dr. Rich Ambrose at UCLA conducted companion monitoring for southern Santa Barbara and Los Angeles Counties. Dr. Jack Engle at the UC Santa Barbara coordinated MARINe efforts, particularly with regards to protocol standardization and documentation. In addition, the BOEMRE Pacific Regional Intertidal Survey and Monitoring (PRISM) Team participated in the sampling, and other program functions to assure continued coordination with BOEMRE was maintained.

SIGNIFICANT CONCLUSIONS:

Ongoing monitoring of the black abalone documented the continuing decline of the species in much of its range. Additional studies coupled to the MARINe monitoring were carried out to determine the extent of the critical habitat for the species. These two data sets were combined to estimate the population size of Black abalone. These results were critical to the listing of the species as endangered.

MARINe datasets were the foundation of the assessment of potential impacts to the State designated Areas of Special Biological Significance.

STUDY RESULTS:

During the course of the performance period for this contract all 24 sites were sampled, usually twice per year (Table 2). Both sessile and motile species were sampled and sampling was generally uneventful. Fourteen target species were sampled across the project sites and in many of these plots, motile species were also sampled. During this period no additional sites were set up using direct BOEMRE funding, but 38 sites were set up using co-funding from the State of California (MPA and ASBS funding) and the U.S. Fish and Wildlife Service.

During this period MARINe protocols were accepted as the first approved monitoring protocol for the U.S. National Park Service monitoring program (for Redwoods National

5 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

Park), and these protocols are now being used as the basis of monitoring programs in Park Service areas on the east coast.

In terms of the biological communities sampled, the major result is the continued decline in the black abalone. The decline during this period was more muted than in the past, but still present. Importantly recruitment of new individuals still has not occurred at sites affected severely by the withering disease. Other species were dynamic but the changes in populations were not outside natural dynamics. We continued to monitor invasive species, but did not note any additional invasions. A full data report covering all MARINe sites will be finished in 2011. This report will be a comprehensive assessment of the entire MARINe region and cover species dynamics at spatial scales from 1000’s to 10’s of kilometers and temporal scales from seasons to decades. This will be the most comprehensive assessment of a marine ecosystem (rocky intertidal throughout much of the California Current region) ever done.

STUDY PRODUCT(S): Products include annual update of the MARINe database, collection and archival of photos and specimens, 135 conference presentations, 39 peer reviewed papers and posters, and 25 reports. See report and www.MARINe.gov for full listing.

6 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

FINAL STUDY REPORT

PART I: INTRODUCTION, OBJECTIVES, AND APPROACH

1.1 Introduction The central/southern California mainland and Channel Islands seacoasts possess an exceptional diversity of valuable rocky intertidal resources. Major factors contributing to the richness of coastal marine life in this region include their location along the boundary of two major biogeographic provinces (cold-temperate Oregonian and warm-temperate Californian), their high diversity of habitat types, and their exposure to varying local oceanographic conditions. In addition, these rocky intertidal resources are heavily utilized (Thompson et al. 1993), with large human populations concentrated on the coastlines of San Diego, Orange and Los Angeles Counties. Oil and gas activities, especially the tankering of oil along the California coast and the extraction of oil from Outer Continental Shelf (OCS) activities, raise the possibility of an oil spill or other impact to coastal resources. Population monitoring of coastal biota in central and southern California would provide baseline information in case an event such as a spill damaged these resources. This baseline information would be essential for (1) scientific studies investigating the short- and long-term effects of the spill, and (2) natural resource damage assessment. In addition, the monitoring studies would yield important data on population dynamics on a local and regional scale, which could be utilized for more effective resource management as well as provide fundamental ecological knowledge about the dynamics of the systems.

Federal, state and local agencies have recognized the importance of baseline information on coastal ecological resources by funding the establishment of a network of monitoring stations noted above. Of the over 120 established MARINe sites, over half are funded by Federal agencies, (e.g., BOEMRE, The National Park Service), and the balance are funded by private, State, and non-governmental entities. The biological information acquired during these surveys also is incorporated into resource databases hosted by the Multi-Agency Rocky Intertidal Network (MARINe) and Partnership for Interdisciplinary Study of Coastal Oceans (PISCO). This innovative monitoring program was initiated by the Channel Islands National Park in the early 1980’s (Davis 1985; Richards and Davis 1988). In 1990, the Cabrillo National Monument in San Diego County began long-term rocky intertidal monitoring (Davis and Engle 1991). Monitoring in Santa Barbara County began in 1992 with a project funded jointly by the Bureau of Ocean Energy Management (BOEMRE), formerly the Minerals Management Service (MMS), which funded monitoring of intertidal and subtidal resources (Ambrose et al. 1992a, b), and the County of Santa Barbara, which funded monitoring of wetland resources (Ambrose et al. 1993). In 1994, it was expanded by the California Coastal Commission (CCC) to include the northern Channel Islands (particularly Santa Cruz Island) and Ventura and Los Angeles Counties (Engle et al. 1994). The CCC projects include monitoring of subtidal, rocky and sandy intertidal and, for Los Angeles/Ventura Counties, wetland resources. Although the monitoring network is principally motivated by oil and gas activities, the information it generates provides valuable information about the status and trends of the

7 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

biological resources of the region, similar to the Environmental Protection Agency (EPA)’s Environmental Monitoring & Assessment Program (EMAP) but on a finer spatial scale. The National Research Council has also emphasized the value of coordinated regional monitoring such as proposed here (NRC 1990a, b).

Nearshore coastal resources can be divided into three general habitat types: intertidal, subtidal, and coastal wetland. All three habitat types could be impacted by an oil spill. Numerous studies have documented major oil spill impacts on rocky intertidal regions (see Foster et al. 1986 for review). Impacts to subtidal habitats are likely to be less (and would certainly be less conspicuous). Coastal wetlands are particularly susceptible to damage from spilled oil; however, many wetlands along the southern California coast are isolated from the open sea during part of the year, or could be protected by booming or diking should a spill occur.

Central and Southern California Rocky Intertidal Habitats

The extent of rocky shoreline varies substantially in central and southern California (Ambrose et al. 1989). The northern section of the region and the Channel Islands are predominantly rocky (Table 1). San Luis Obispo County has the most extensive stretch of rocky shores (54 mi, or 58% of its coastline) in the region, except for the Channel Islands. Ventura and Orange Counties have the least rocky shoreline, each with 3 miles or 7% of the coastline.

Location Coastline Miles Rocky Miles Sandy % Rocky % Length (mi) Sandy San Luis 93 54 39 58 42 Obispo Co. Santa Barbara 110 26 84 24 76 Co.* Ventura Co.* 41 3 38 7 93 Los Angeles 77 26 51 34 66 Co.*^ Orange Co. 41 3 38 7 93 San Diego Co. 76 11 65 14 86 Channel Islands 273 211 62 77 23 * excludes Channel Islands ^ includes harbor breakwaters

Table 1: Extent of rocky and sandy shores for central/southern California. (Mainland data from Littler and Littler, 1979. Island data from Littler and Littler 1980)

The biological communities of the mainland from San Luis Obispo County in the north to Orange County in the south are distinctly different north and south of Point Conception.

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San Luis Obispo and Northern Santa Barbara Counties (north of Point Conception) Rocky intertidal communities to the north of Pt. Conception are well-known for their diverse and relatively pristine biota. The majority of the coast is either privately-owned, owned by the military, or inaccessible and is undeveloped. The natural beauty and coastal resources of this area make it a popular tourist destination, as evidenced by more than 10 State and County Parks and Beaches. A majority of the shore consists of rugged rocky reefs fully or partially exposed to prevailing oceanic swells. Situated at the northern end of the transition zone between southern (Californian) and northern (Oregonian) biota, these intertidal habitats contain a unique mix of species, with warm- temperate species declining and cold-temperate forms increasing in abundance compared with counties to the south. For example, warm-water sea palms (Eisenia arborea), rockweed (Hesperophycus harveyanus), barnacles (Tetraclita rubescens, Chthamalus fissus), and horse mussels (Brachidontes adamsianus) are rare or absent, while cold- water sea palms (Postelsia palmaeformis), rockweed (Fucus distichus, Pelvetiopsis limitata), barnacles (Balanus glandula, Chthamalus dalli), and horse mussels (Septifer bifurcata) appear or increase in abundance in SLO county. Black abalone (Haliotis cracherodii) populations have crashed due to disease, during the period of MARINe monitoring.

The rich marine communities of this region are vulnerable to oil spills or other oil and gas operations impacts, primarily from major coastal tanker traffic, but also from terminal operations at Estero Bay, onshore pipeline breaks, and possible future oil exploration leases. Spills from OCS platforms also pose a threat. The Torch Platform Irene pipeline oil spill in 1997 landed on shores in this region. In addition, other anthropogenic impacts are vastly increasing, particularly those related to increases human access to shores that were until recently only reachable via private ranches. We have noted huge increases in public presence at sites throughout the region, accompanied by harvest and trampling. Only ongoing monitoring is effective at separating such impacts from those that could be linked to oil operations.

Rocky coast flora and fauna in this region remain largely unstudied except for MARINe studies, those done by the PISCO program, impact surveys associated with the Diablo Canyon Nuclear Power Plant located north of Avila Beach (North et al. 1989, Tenera Environmental 1988a, b, 1994) and research on seasonal and successional variation in intertidal community structure conducted at 2 sites (Point Sierra Nevada and Diablo Canyon) (Kinnetic, 1992). The ongoing Diablo Canyon surveys, initiated in the 1970’s, represent an excellent time series for this one area. The seasonal and successional studies at Point Sierra Nevada and Diablo Canyon were funded by BOEMRE, formerly the Minerals Management Service (MMS), during 1985-1991, and currently one of the MARINe sites is at Point Sierra Nevada, thus extending the period of sampling to 2010.

9 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

Southern Santa Barbara, Ventura, Los Angeles and Orange Counties (south of Pt. Conception) This region is prominent in the distribution of rocky intertidal organisms because it is bordered by Point Conception, an important biogeographical transition area. Although there is considerable overlap, there are distinct differences between the organisms north and south of Point Conception (Murray and Littler 1981, Ambrose et al., 1992a, b). For example, seaweed communities north of Point Conception are characterized by species such as Laminaria, lean brown algae and large, fleshy red algae, and by greater biomass, whereas communities south of the Point are characterized by fucalean brown algae and shorter, more densely branched red algae (Abbott and Hollenberg 1976).

Concerns about the impact of oil spills in this region stem from transport by offshore tanker and onshore pipeline, production platforms, and terminal operations. Natural oil seeps are prominent features, especially at Point Conception. Previous studies in the region include work by PISCO, Littler and colleagues at Coal Oil Point and Government Point (Littler 1979), funded by BOEMRE, and Kinnetics at Government Point.

1.2 Objectives The primary objective for this research was to contribute to the ongoing monitoring program that provides a basis for determining if change in rocky shoreline communities adjacent to producing OCS facilities can be attributed to producing operations or accidents from OCS facilities. The second objective was to provide an ecological context through monitoring so as to understand the natural and anthropogenic changes to these communities that have occurred in the Southern California Bight since the OCS program was initiated. This latter objective is based on collaboration between MARINe and other groups (especially PISCO) and includes the collection of additional biodiversity data and comparison to comparable historic data (using matching funds). Additional objectives included oversight of a concurrent database process and publication of metadata for the BOEMRE-funded long term data set.

1.3 Approach The work completed in the period 2007-2010 employed methodologies consistent with the previous MARINe projects in order to maximize comparability among project results. The methodological details for these projects can be found in Engle (2005 and www.marine.gov), and are summarized below.

Target Species Monitoring To accomplish the first objective, target species at 24 established rocky intertidal sites along the mainland coast of Southern and Central California adjacent to producing platforms were monitored spring and fall (Table 2, Figure 1).

10 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

North/South Principal Site Name SiteID Order Group Investigator Seasons Sampled Point Sierra Nevada PSN 1 UCSC Pete Raimondi 2007 Spring to 2010 Fall Piedras Blancas Lighthouse PBL 2 UCSC Pete Raimondi 2007 Spring to 2010 Fall Rancho Marino Reserve RMR 3 UCSC Pete Raimondi 2007 Spring to 2010 Fall Cayucos CAY 4 UCSC Pete Raimondi 2007 Spring to 2010 Fall Hazards HAZ 5 UCSC Pete Raimondi 2007 Spring to 2010 Fall Shell Beach SHB 6 UCSC Pete Raimondi 2007 Spring to 2010 Fall Occulto OCC 7 UCSC Pete Raimondi 2007 Spring to 2010 Fall Purisima PUR 8 UCSC Pete Raimondi 2007 Spring to 2010 Fall Stairs STA 9 UCSC Pete Raimondi 2007 Spring to 2010 Fall Boathouse BOA 10 UCSC Pete Raimondi 2007 Spring to 2010 Fall Government Point GPT 11 UCSC Pete Raimondi 2007 Spring Alegria ALEG 12 UCLA Rich Ambrose 2007 Spring to 2010 Fall Arroyo Hondo ARHO 13 UCLA Rich Ambrose 2007 Spring to 2010 Fall Coal Oil Point COPT 14 UCLA Rich Ambrose 2007 Spring to 2010 Fall Carpinteria CARP 15 UCLA Rich Ambrose 2007 Spring to 2010 Fall Mussel Shoals MUSH 16 UCLA Rich Ambrose 2007 Spring to 2010 Fall Old Stairs OLDS 17 UCLA Rich Ambrose 2007 Spring to 2010 Fall Paradise Cove PCOV 18 UCLA Rich Ambrose 2007 Spring to 2010 Fall Whites Point WHPT 19 UCLA Rich Ambrose 2007 Spring to 2010 Fall Point Fermin PTFM 20 UCLA Rich Ambrose 2007 Spring to 2010 Fall Crystal Cove CRCO 21 CSUF Steve Murray 2007 Spring to 2010 Fall Shaws Cove SHCO 22 CSUF Steve Murray 2007 Spring to 2010 Fall Treasure Island TRIS 23 CSUF Steve Murray 2007 Spring to 2010 Fall Dana Point DAPT 24 CSUF Steve Murray 2007 Spring to 2010 Fall

Table 2: Sites sampled from north to south, group and Principle Investigator (PI) responsible for sampling and the seasons that were sampled during the contractual period.

11 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

Location of sampling sites

Figure 1: Locations of sampling sites

Figure 1: Location of Sampling Sites

Target species include: mussels (Mytilus californianus), barnacles (Chthamalus spp., Balanus glandula and Pollicipes polymerus), anenomes (Anthopleura elegantissima), algal species including Endocladia muricata, Hesperophycus harveyanus, Silvetia compressa, Mazzaella spp., Mastocarpus papillatus, surfgrass (Phyllospadix scouleri/torreyi), motile invertebrates such as owl limpets (Lottia gigantea), black abalone (Haliotis cracherodii) and sea stars (Pisaster ochraceus). Table 3 shows the target species at each of the sites sampled. Table 4 shows the plots in which motile species were also sampled. Analysis following the 167 bbl. “Torch spill”, an OCS

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pipeline spill from the Platform Irene pipeline, showed that it was possible to detect change in percent cover of barnacles and mussels as small as 8-15% using this fixed plot sampling protocol. Importantly, it was also possible to differentiate between natural changes such as the El Nino storms and the effects of the oil spill (Raimondi et. al, 1999). It is vital that the monitoring protocol is in sufficient detail to address these low-level changes.

Mussels, barnacles, anenomes and algal species were photographed in fixed rectangular plots and scored in the lab or field (barnacles at some sites) by scoring species under 100 points on each slide. Five replicate plots per target species were photographed at each site where the plots occurred. Surfgrass cover was estimated using a point contact method along 10-meter long transects. Owl limpets were measured and counted in five replicate, 1-meter circular plots at each site where the plots occurred. Abalone were counted and measured in three replicate irregular plots. Sea stars were counted, measured and classed by color in either 2-meter wide, 10-meter long band transects or irregular plots, depending on the habitat. In many of the target species plots, we also sampled the associated motile species (Table 4). To optimize future environmental impact assessments, sites have been established systematically over a broad geographic range and each species is monitored at several sites within that range.

Monitoring of the long-term sites was usually done in Fall and Spring each year, although the motile species in target species plots were sometimes sampled only once per year (see Table 4). There can be considerable seasonal changes in the rocky intertidal community, especially after stormy winters and hot summers. Two samples per year adequately track these communities. October or November is usually the first period after summer with low tides during the daytime (which greatly improve efficiency of sampling and safety), and is appropriate for determining the post-summer community. March or April is an appropriate time to determine the post-winter community, and there are once again low tides during the daytime.

13 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

Target Species

Site Name anthopleura chthamalus/b alanus endocladia haliotis hesperophycus lottia mastocarpus mazzaella mytilus pisaster pollicipes postelsia recovery silvetia Point Sierra Nevada X XX XXXX X X Piedras Blancas Lighthouse XX XXXXX Rancho Marino Reserve XX Cayucos XXXXX XX X Hazards XX X XXX X Shell Beach XX X XX X Occulto XX XX Purisima X Stairs XXX X XX XX Boathouse XXXX X XX X Government Point XXX X XXX X Alegria XX X XXX Arroyo Hondo XXX Coal Oil Point XX Carpinteria XX X XXX Mussel Shoals XX X XX Old Stairs XXX X XX Paradise Cove XX X XX Whites Point XX X XX Point Fermin XXXXX Crystal Cove XXXXX Shaws Cove XX X XX X Treasure Island XXXX Dana Point XXXXX

Table 3: Target species sampled (X) at each of the 24 sample sites.

14 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

Target Species

Motile Sampling Notes Site Name chthamalus / balanus endocladia hesperophycus mastocarpus mytilus pollicipes recovery silvetia Crystal Cove XXX Dana Point XXX Shaws Cove XX X X Treasure Island XXX Piedras Blancas Lighthouse XXXXSpring sampling only Alegria X XX Spring sampling only Arroyo Hondo X X Spring sampling only Carpinteria X XX Spring sampling only Coal Oil Point X Spring sampling only Mussel Shoals X X Spring sampling only Old Stairs XX X Spring sampling only Paradise Cove XX X Spring sampling only Point Fermin X X X Spring sampling only Whites Point XX X Spring sampling only Boathouse XX X X Cayucos XXX X X Government Point XX X X Hazards XX X X Occulto XX X No Fall 2007 sampling Point Sierra Nevada XXX X Shell Beach XX XX X Stairs XX X X X No Fall 2007 sampling

Table 4: Target species plots in which motile organisms were sampled

15 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

Depending on the size of the site and the number of target species being monitored, one pair to three pairs of biologists was needed to collect the field data. The majority of sites needed four to five trained biologists to complete the work on a given tide. Pacific Region Intertidal Survey and Monitoring (PRISM) Team, formerly MMS Intertidal Team (MINT) biologists assisted in the collection of the field data at as many as 20 of the sites depending on tidal cycles. Travel to and from sites benefited from cost sharing since several sites can be surveyed during one tide cycle.

Protocols used to collect the data were standardized, coordinated with other members of MARINe, and were not altered without prior approval of BOEMRE. A base protocol was standardized across the Bight among MARINe members and was maintained at each site; additional protocols needed to address site specific problems or answer species- specific questions were sometimes added with BOEMRE approval. Additional protocols which did not add field costs overall were accommodated in order to address these important research questions, so long as this was coordinated properly with MARINe members.

This collection of field data was carried out by the University of California, Santa Cruz (UCSC), University of California, Los Angeles (UCLA), and California State University, Fullerton (CSUF) (see Table 2).

Coordination—Internal and with MARINe

Since several teams of biologists were needed to collect data at over 120 established sites (including the 24 covered in this grant proposal), coordination among field teams was essential to ensure that the data collected was of the highest quality and is comparable across sites. Therefore, strong coordination was needed between the Principal Investigators (PI)’s to ensure continuity since the tasks were inherently integrated between Universities. This coordination included regular meetings, email, phone calls and joint participation in the field. This ensured that individual PI’s are not inadvertently making changes in protocols or data processing which affect the other PI’s.

Strong coordination was also needed between BOEMRE and MARINe to ensure that BOEMRE was providing data in a timely fashion to MARINe and that MARINe products directly met the needs of the scientists, including the BOEMRE PI’s. BOEMRE committed to providing a MARINe coordinator to that end. The duties of the coordinator included:

1. Facilitating the development of the database by: a. Acting as a liaison between the database consultant and MARINE researchers in developing timely responses to database questions. b. Coordinating with the BOEMRE researchers in particular and MARINE researchers in general to ensure their data and metadata inputs are complete and timely.

16 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

c. Providing a broad range of knowledge regarding the MARINE sites and technical issues to the database consultant to ensure that the database will be useful to researchers when it is completed. 2. Organizing and moderating biannual Steering Committee, Science Panel and Database Panel meetings for MARINe. 3. Providing ongoing coordination with the MARINe committee representatives and organizations outside MARINe to facilitate continued long-term funding of MARINe sites. 4. Working with MARINe to develop automated standardized field datasheets. 5. Working with MARINe to reach agreement and develop procedures which promote timely release of data to the public.

These tasks were done at all campuses but the responsibility for coordination was centered at the University of California, Santa Barbara (UCSB).

Data management Data management was overseen at UCSC. Duties included administering data in the MARINe (access) database. All campuses were responsible for uploading data using data forms, but no alterations to the database were be made without approval from the data administrator. Data were accessible via the Microsoft Access relational database management system interface, and revisions were made approximately twice per year. Data are available to all agencies and interested parties that make specific requests.

Project management The UCSC portion of the program was managed by the Principal Investigator, Dr. Pete Raimondi. Dr. Raimondi has been a Principal Investigator of the BOEMRE-funded rocky intertidal inventory project since its inception and has been responsible for data analysis of the project for the past ten years. Dr. Raimondi was responsible for overseeing financial aspects of the project, and in particular was responsible for ensuring completion of project objectives and deliverables. This was done, in part, through coordination meetings and conference calls. However the main means of ensuring performance was through the yearly workshops where all PI’s get together along with staff to review the status of the project.

Because this proposal is part of an overall coordinated monitoring program, the work was closely coordinated with other aspects of that program. Overall coordination was led by Dr. Steve Murray and Jayson Smith at CSUF, who conducted similar monitoring in Orange County. Dr. Rich Ambrose at UCLA conducted companion monitoring for southern Santa Barbara and Los Angeles Counties. Dr. Jack Engle at the UCSB coordinated MARINe efforts, particularly with regards to protocol standardization and documentation. In addition, the BOEMRE PRISM Team participated in the sampling, and other program functions to assure continued coordination with BOEMRE was maintained.

17 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

1.4 Significant Conclusions Ongoing monitoring of the black abalone documented the continuing decline of the species in much of its range. Additional studies coupled to the MARINe monitoring were carried out to determine the extent of the critical habitat for the species. These two data sets were combined to estimate the population size of black abalone. These results were critical to the listing of the species as endangered.

MARINe monitoring data was used by the State of California to aid in the Marine Life Protection Act design of the Marine Protected Area (MPA) network for southern California. Intertidal datasets were used to delineate the biogeographic regions and optimal sizes of intertidal MPA’s were also calculated based on MARINe datasets. MARINe datasets were the foundation of the assessment of potential impacts to the State designated Areas of Special Biological Significance (ASBS).

1.5 Study Results During the course of the performance period for this contract all 24 sites were sampled, usually twice per year (Table 2). Both sessile and motile species were sampled and sampling was generally uneventful. Fourteen target species were sampled across the project sites and in many of these plots, motile species were also sampled. During this period no additional sites were set up using direct BOEMRE funding, but 38 sites were set up using co-funding from the State of California (MPA and ASBS funding) and the U.S. Fish and Wildlife Service.

During this period MARINe protocols were accepted as the first approved monitoring protocol for the U.S. National Park Service monitoring program (for Redwoods National Park), and these protocols are now being used as the basis of monitoring programs in Park Service areas on the east coast.

In terms of the biological communities sampled, the major result is the continued decline in the black abalone. The decline during this period was more muted than in the past, but still present. Importantly, recruitment of new individuals still has not occurred at sites affected severely by the withering disease. Other species were dynamic but the changes in populations were not outside natural dynamics. We continued to monitor invasive species, but did not note any additional invasions. A full data analysis report covering all MARINe sites will be finished in 2011. This report will be a comprehensive assessment of the entire MARINe region and cover species dynamics at spatial scales from 1000’s to 10’s of kilometers and temporal scales from seasons to decades. This will be the most comprehensive assessment of a marine ecosystem (rocky intertidal throughout much of the California Current region) ever done.

1.6 Study Product(s) Products include the following: continual enhancements to the MARINe Database; launch of a completely revamped public MARINe website, (which includes current news

18 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010) and research); restructuring of the private website (in progress); online availability of all MARINe data on www.piscoweb.org, (including data not previously included in the Access Database); the update of the MARINe Handbook, including updated tables and protocol enhancements; archival of photos and specimens; conference presentations, peer reviewed papers and posters, and reports; and organization and recording of data and info requests. Listed below are products of MARINe during this period; starred items were produced either using BOEMRE funding, using data collected at BOEMRE funded sites, or presented at a BOEMRE funded workshop.

Presentations (2007-2010) *Ambrose, R. 2007. Oil spill rapid response protocols. MARINe Annual Workshop, San Francisco, CA. *Ambrose, R. 2007. Public access versus resource protection. MARINe Annual Workshop, San Francisco, CA. Ammann, K.N. 2010. Long-term rocky intertidal monitoring of Redwood National and State Parks. Presentation for National Park Service Klamath Network Inventory and Monitoring Program-Three Year Program Review. *Ammann, K.N., C.A. Bell. M.K. George, and P.T. Raimondi. 2009. An overview of the biological sampling used to assess the central California coast marine protected areas – with emphasis on rocky intertidal habitats. Western Society of Naturalists Annual Meeting, Monterey, CA. *Anderson, D. 2009. Survey team monitoring summary: Northern CA/Oregon. MARINe Annual Workshop, San Francisco, CA. *Anderson, L. 2009. Survey team monitoring summary: Santa Barbara/San Luis Obispo Counties. MARINe Annual Workshop, San Francisco, CA. Augyte, S. and F.J. Shaughnessy. 2010. A preliminary floristic analysis of marine intertidal algae from Cape Mendocino, CA to Cape Blanco, OR. Western Society of Naturalists Annual Meeting, San Diego, CA. *Bell, C. 2007. Digital photo archive - where are we now and where are we headed? MARINe Annual Workshop, San Francisco, CA. *Bell, C. 2008. Go-kit protocol demonstration and what we learned from the Cosco Busan Oil Spill. MARINe Annual Workshop, San Pedro, CA. *Bell, C. 2008. Optional protocols revisited. MARINe Annual Workshop, San Pedro, CA. *Bell, C.A., K.N. Ammann, M.K. George, and P.T. Raimondi. 2009. Assessing the amount of suitable habitat and the population size of black abalone (Haliotis cracherodii) from Half Moon Bay to Point Conception. Western Society of Naturalists Annual Meeting, Monterey, CA; Black Abalone Critical Habitat Meeting, Ventura, CA; and MARINe Annual Workshop, San Francisco, CA. *Bell, C.A., K.N. Ammann, M.K. George, and P.T. Raimondi. 2010. Assessing suitable habitat and the population size of black abalone (Haliotis cracherodii) for critical habitat designation. Poster at Western Society of Naturalists Annual Meeting, San Diego, CA. Bell, Christy. 2007. The importance of community structure and biodiversity surveys to establish baseline data for Marine Reserves. COBI Fishing CO-OP meeting, Isla Natividad, Baja California Sur, Mexico. *Blanchette, C. 2009. Biodiversity survey overview. MARINe Annual Workshop, San Francisco, CA.

19 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

Blanchette, C.A. 2007. Intertidal communities of the CA Channel Islands: ecology and natural history. Western Society of Naturalists Annual Meeting, Ventura, CA. Blanchette, C.A., P.T. Raimondi, and B. R. Broitman. 2008. Spatial patterns of intertidal community structure across the California Channel Islands and links to ocean temperature. 7th California Islands Symposium, Oxnard, CA. *Conway-Cranos, L. 2007. Geographic patterns of recovery in intertidal communities. Partnership for Interdisciplinary Studies of Coastal Oceans (PISCO) Scientific Symposium. Corvallis, OR. *Conway-Cranos, L. 2007. Prediction and understanding the recovery of communities: An example from the rocky intertidal. Pacific Ecology and Evolution Conference. Seattle, WA; and Ecological Society of America Annual Conference. San Jose, CA. *Conway-Cranos, L. 2010. An investigation of the relative importance of mechanisms driving variation in the recovery of mussel beds. Western Society of Naturalists Annual Meeting, San Diego, CA. *Conway-Cranos, L. 2010. Recovery dynamics in rocky intertidal communities: An experimental evaluation of resilience. Seminar at Friday Harbor Marine Laboratory, University of Washington, WA. *Conway-Cranos, L.. 2009. Recovery dynamics in rocky intertidal communities: Patterns, mechanisms and simulations. Ecological Society of America Annual Conference, Albuquerque, NM and Bodega Marine Laboratory Seminar. *Conway-Cranos, L.L. 2008. Facultative interactions as a potential driver for spatial variation in recovery patterns in the California rocky intertidal. Western Society of Naturalists Annual Meeting, Vancouver, BC. *Conway-Cranos, L.L. 2008. Recovery of intertidal communities: Perspectives from a broad-scale manipulation. MARINe Annual Workshop, San Pedro, CA. *Cox, K. 2007. MARINe regional sampling update: Northern California. MARINe Annual Workshop, San Francisco, CA. *Dalkey, A. and B. Allen. 2008. Palos Verdes Peninsula: research and education opportunities. MARINe Annual Workshop, San Pedro, CA. *Douros, W. 2007. MARINe, marine sanctuaries and more. MARINe Annual Workshop, San Francisco, CA. *Eernisse, D. 2008. Common chitons and limpets of southern California rocky intertidal. MARINe Annual Workshop, San Pedro, CA. Elsberry, L.A. and J.L. Burnaford. 2010. The effects of low-tide exposure on the high intertidal alga Endocladia muricata in two geographic regions. Poster at Western Society of Naturalists Annual Meeting, San Diego, CA. *Engle, J. 2007. Multi-Agency Rocky Intertidal Network status. MARINe Annual Workshop, San Francisco, CA. *Engle, J. 2007. The Light and Smith Manual: invertebrate name changes. MARINe Annual Workshop, San Francisco, CA. *Engle, J. 2008. MARINe aids NOAA Mussel Watch expansion in southern California. MARINe Annual Workshop, San Pedro, CA. *Engle, J. 2008. Multi-Agency Rocky Intertidal Network status. MARINe Annual Workshop, San Pedro, CA. *Engle, J. 2009. Multi-Agency Rocky Intertidal Network status. MARINe Annual Workshop, San Francisco, CA.

20 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

Fenberg, P.B. and K. Roy. 2007. The ecological consequences of size-selective harvesting: the owl limpet (Lottia gigantea) as a case study. Western Society of Naturalists Annual Meeting, Ventura, CA. Flectcher, N.C., P.T. Raimondi, C.M. DaCosta, M.A. Redfield, and S.E. Worden. 2010. Poster at Western Society of Naturalists Annual Meeting, San Diego, CA. *Fong, D. 2009. MARINe sites on Alcatraz. MARINe Annual Workshop, San Francisco, CA. *Gaddam, R. 2008. Biodiversity surveys and PISCO updates. MARINe Annual Workshop, San Pedro, CA. *Gaddam, R. 2009. Accessing MARINe data through the online PISCO data catalog. MARINe Annual Workshop, San Francisco, CA. Garza, M.M. 2010. Relationship between habitat complexity and ochre sea star (Pisaster ochraceus) abundance. Poster at Western Society of Naturalists Annual Meeting, San Diego, CA. *George, Maya, Christy Bell, Karah Ammann and Peter Raimondi. 2009. Assessing the amount of suitable habitat and the population size of black abalone from Half Moon Bay to Point Conception. Poster at Monterey National Marine Sanctuary Symposium, Monterey, CA. *Gilbane, L. and J. Smith. 2008. MARINe training video. MARINe Annual Workshop, San Pedro, CA. *Gilbane, L. and S. Kimura. 2009. Mapping: quest for the perfect map. MARINe Annual Workshop, San Francisco, CA. *Gray, H. 2008. Common shorebirds of southern California rocky shores. MARINe Annual Workshop, San Pedro, CA. *Gregorio, D. 2007. Areas of Special Biological Significance and MARINe. MARINe Annual Workshop, San Francisco, CA. *Gregorio, D. and K. Schiff. 2008. California Areas of Special Biological Significance. MARINe Annual Workshop, San Pedro, CA. Hays, CG. 2008. Genetic and maternal variation across a species’ distribution: consequences for emersion tolerance in an intertidal alga. Seminars at California State University Sacramento; Sacramento, CA; and California State University San Jose; San Jose, CA. Hays, CG. 2010. Genetic and maternal variation across a species’ distribution: consequences for emersion tolerance in an intertidal alga. Seminar at Moss Landing Marine Lab, Moss Landing, CA. *Helix, M.E. 2007. Overview of Multi-Agency Rocky Intertidal Network. MARINe Annual Workshop, San Francisco, CA. *Helix, M.E. 2007. Rocky Intertidal Monitoring Network and the Southern California Coastal Ocean Observing System. SCCOOS Board of Governors Meeting June 13, 2007. *Helix, M.E. 2008. Overview of Multi-Agency Rocky Intertidal Network. MARINe Annual Workshop, San Pedro, CA. *Helix, M.E. 2009. Overview of Multi-Agency Rocky Intertidal Network. MARINe Annual Workshop, San Francisco, CA. *Helix, M.E. 2010. Long-term monitoring program challenges – MARINe, the Multi-Agency Rocky Intertidal Network. Southern California Academy of Sciences Annual Meeting, Los Angeles, CA. *Helix, M.E., P. Raimondi, R. Ambrose, J. Engle, and S. Murray. 2007. MARINe: examining the health of rocky shores along the Pacific Coast. Monterey Bay National Marine Sanctuary Currents Symposium, Monterey, CA. *Helix, M.E., R.F. Ambrose, J.M. Engle, S.N. Murray, and P.T. Raimondi. 2007. Examining the health of rocky shores along the Pacific Coast – can local government and citizen’s help? Coastal Zone 2007, Portland, OR.

21 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

Hewson, W.E. and D.J. Eernisse. 2007. A common southern California limpet is a new species that overlaps with its sister species in northern Baja California. Western Society of Naturalists Annual Meeting, Ventura, CA. *Joab, B. and J. Cubit. 2008. MARINe and NRDA’s: increasing the effectiveness of the combination. MARINe Annual Workshop, San Pedro, CA. *Jones, A.M. and D.P. Lohse. 2009. A regional comparison of Mytilus californianus growth rates along the central coast of California. Western Society of Naturalists Annual Meeting, Monterey, CA. *Kimura, S. 2007. GIS maps of the California coastline. MARINe Annual Workshop, San Francisco, CA. *Kinyon, J. 2009. Habitat mapping in Golden Gate National Recreation Area. MARINe Annual Workshop, San Francisco, CA. *Lawrenz-Miller, S. 2008. Long term intertidal population surveys on the Palos Verdes Peninsula. MARINe Annual Workshop, San Pedro, CA. *Lee, S. 2008. MARINe site at Point Fermin. MARINe Annual Workshop, San Pedro, CA. *Lee, S. 2008. Multi-Agency Rocky Intertidal Network. Teacher Training Workshop for Center for Ocean Sciences Education Excellence (COSEE-West), San Pedro, CA. *Lee, S. 2009. Survey team monitoring summary: LA/Ventura Counties. MARINe Annual Workshop, San Francisco, CA. *Livingston, H. 2009. Species ranges: climate change implications. MARINe Annual Workshop, San Francisco, CA. *Long, J. 2007. MARINe on the East Coast. MARINe Annual Workshop, San Francisco, CA. *Long, J. 2008. MARINe on the East Coast. MARINe Annual Workshop, San Pedro, CA. *Long, J. 2009. Survey team monitoring summary: East Coast. MARINe Annual Workshop, San Francisco, CA. *Lonhart, S. 2007. MARINe regional sampling update: Central California. MARINe Annual Workshop, San Francisco, CA. *Maloney, E. 2008. California Introduced Species Surveys: who’s on our turf? MARINe Annual Workshop, San Pedro, CA. Maloney, E.R., W.R. Fairey, A.A. Lyman, Z.A. Walton, S.F. Foss, and S.N. Shiba. 2008. Surveys for introduced marine species on the outer coast of California: who’s on our turf? Western Society of Naturalists Annual Meeting, Vancouver, BC. *Miller, K.A. 2009. Invasive species status. MARINe Annual Workshop, San Francisco, CA. Miller, K.A. 2010. California’s non-native seaweeds: a case study. XX International Seaweed Symposium, Ensenada, Baja California, Mexico. *Miner, C.M. 2008. MARINe database structure. MARINe Meeting, Seattle, WA *Miner, C.M. 2008. MARINe Rocky Intertidal Monitoring Program, Northwest Straits Initiative Meeting, Bellingham, WA *Miner, M. 2007. Multi-Agency Rocky Intertidal Network database update. MARINe Annual Workshop, San Francisco, CA. *Miner, M. 2008. Multi-Agency Rocky Intertidal Network database update. MARINe Annual Workshop, San Pedro, CA. *Miner, M. 2009. Survey team monitoring summary: Washington State. MARINe Annual Workshop, San Francisco, CA.

22 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

Monaco, C.J. 2010. Size-dependent intertidal distribution and foraging behavior in Pisaster ochraceus. Poster at Western Society of Naturalists Annual Meeting, San Diego, CA. *Murray, S. 2007. Science, politics, the public and protecting California’s coastal ecosystems. Southern California Academy of Sciences Annual Meeting, Fullerton, CA. *Murray, S. 2008. Changes in rocky intertidal communities on the Channel Islands and the southern California mainland since the 1970’s. 7th California Islands Symposium, Oxnard, CA. *Murray, S., R.F. Ambrose, J. Engle, P. Raimondi, and S. Weisberg. 2010. Developing indicators for monitoring the status of rocky shores. California and the World Ocean 2010 Conference, San Francisco, CA. *Murray, S.N., C.A. Navarro, S.C. Vogt, and J.R. Smith. 2010. Feeding responses of native macro- invertebrates to non-indigenous seaweeds. XX International Seaweed Symposium, Ensenada, Baja California, Mexico. *Murray, S.N., J. R. Smith, A. Bullard, and L. Gilbane. 2009. Changes in Coastal Seaweed Populations over time in Urban Settings and the Ecological Implications (Plenary Lecture). Novos Bioativos de Macroalgas Workshop, Ilhabela – São Paulo, Brazil. *Murray. S. N. 2008. Seaweed Introductions: An Overview. Control of Invasive Marine Seaweeds Workshop, Asilomar, CA. *Navarro, C. 2007. MARINe regional sampling update: Southern California. MARINe Annual Workshop, San Francisco, CA. *Navarro, C.N., J.R. Smith, and S.N. Murray. 2007. Feeding rates of native consumers on introduced and native seaweeds on urban southern California shores. Southern California Academy of Sciences Annual Meeting, Fullerton, CA. *Neuman, M.J. and G.R. VanBlaricom. 2008. Status of black abalone populations at the California Channel Islands: implications for long-term viability throughout the range of the species. 7th California Islands Symposium, Oxnard, CA. Orr, D., P. Raimondi, C. Bell, T. Conway-Cranos, M. George, D. Lohse, and S. Worden. 2010. Assessment of effect and predictions of recovery dynamics when baseline data are scarce: a case study of the Cosco Busan oil spill. Western Society of Naturalists Annual Meeting, San Diego, CA. *Orr, D.W., M.A. Redfield, L.M. Anderson, K.N. Ammann. 2010. Overview of the biological sampling used to assess California’s Central Coast Marine Protected Areas – with an emphasis on rocky intertidal habitats. Poster at Monterey Bay National Marine Sanctuary Symposium, Monterey, CA. Parker, M.A. and K.J. Nielsen. 2007. A tale of two headlands: recruitment and reproductive output of Balanus glandula and Chthamalus dalli along the northern California coast. Western Society of Naturalists Annual Meeting, Ventura, CA. Pearse, J.S., D.E. Pearse, and V.B. Pearse. 2007. Rising sea level and changes in intertidal zonation: professor Snadrock 60 years later. Western Society of Naturalists Annual Meeting, Ventura, CA. Pister, B. and T. Philippi. 2010. Twenty years of rocky intertidal monitoring at Cabrillo National Monument: detection and analysis of long-term trends. Western Society of Naturalists Annual Meeting, San Diego, CA. *Protopapadakis, L. 2008. California’s Marine Life Protection Act: laying a foundation for the future. MARINe Annual Workshop, San Pedro, CA. *Raimondi, P. 2007. MARINe and Marine Protected Areas. MARINe Annual Workshop, San Francisco, CA.

23 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

*Raimondi, P., D. Gregorio, and A. Compton. 2007. Rocky intertidal health. MARINe Annual Workshop, San Francisco, CA. *Raimondi, P.T. 2008. Go-kit protocols updated through Cosco Busan Experience. MARINe Annual Workshop, San Pedro, CA. Recchia, C., L. Whitman, P. Raimondi, A. Scholz, S. Murray, and S. Katz. 2010. Evolving MPA monitoring: aligning science and policy. California and the World Ocean 2010 Conference, San Francisco, CA. *Redfield, M. 2009. Survey team monitoring summary: Monterey/Marin Counties. MARINe Annual Workshop, San Francisco, CA. Redfield, M.A., P.T. Raimondi, N.C. Fletcher, and S.E. Worden. 2010. An overview of the North Central Coast Marine Protected Areas Baseline Program monitoring. Poster at Western Society of Naturalists Annual Meeting, San Diego, CA. Reinhard, L.J., K.N. Ammann, M.T. Tinker, P.T. Raimondi, and C.A. Bell. 2009. Effects of sea otters on local distribution and density of black abalone. Western Society of Naturalists Annual Meeting, Monterey, CA. Richards, D. 2008. Foundations of Marine Reserves at the Channel Islands, NPS Aquatic Professionals Meeting, Fort Collins, CO. *Richards, D. 2009. Black abalone restoration/recovery plan status. MARINe Annual Workshop, San Francisco, CA. Richards, D. 2009. Marine Reserves at the Channel Islands. George Wright Society Meeting, Portland, OR. *Richards, D. 2009. Survey team monitoring summary: Channel Islands. MARINe Annual Workshop, San Francisco, CA. Richards, D.V. 2008. Black abalone at the Channel Islands, a brief history. 7th California Islands Symposium, Oxnard, CA. Richards, D.V. and S.G. Whitaker. 2010. Monitoring black abalone movement and aggregating behavior. Poster at Western Society of Naturalists Annual Meeting, San Diego, CA. Sagarin, R.D. 2008. Size matters: loss of large coastal invertebrates and implications for ecology and management. Western Society of Naturalists Annual Meeting, Vancouver, BC. *Smith, J.R. 2007. Long-term change in macrophyte & macroinvertebrate communities on wave-exposed rocky intertidal shores. Seminar at California State University, Northridge, Department of Biology, Biology Colloquium. *Smith, J.R. 2007. Seaweed communities in a heavily urbanized environment in southern California. Seminar at the Coastal Studies Consortium, Universidade Federal Fluminense, Niteroi, Brazil. *Smith, J.R. 2008. Coastal ecology in the face urbanization and environmental change. Seminars at Eastern Connecticut State University, and NOAA Workshop on Managing Visitor Use at Dana Point, CA. *Smith, J.R. 2009. Coastal urban ecology for teachers. Seminar for Centers for Ocean Sciences Education Excellence (COSEE) at Dana Point, CA. *Smith, J.R. 2009. Survey team monitoring summary: San Diego/Orange Counties. MARINe Annual Workshop, San Francisco, CA. *Smith, J.R. 2009. Urban ecology: a southern California rocky intertidal perspective. Seminars at SUNY Stony Brook Southampton, NY, CA State University Fullerton, and University of Alaska Southeast. *Smith, J.R. 2010. Urban ecology: a southern California rocky intertidal perspective. Seminars at California Polytechnic University, CA and University of New Haven, CT.

24 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

*Smith, J.R., R.F. Ambrose, and P. Fong. 2008. Regional comparisons and decadal changes in mussel populations (Mytilus californianus) and mussel bed community diversity along the California coast. 7th California Islands Symposium, Oxnard, CA. *Smith, J.R., S.G. Whitaker, and S.N. Murray. 2009. Experimental re-establishment of the rockweed, Silvetia compressa, on urban southern California shores. Western Society of Naturalists Annual Meeting, Monterey, CA. Smith, K.A. and B. Helmuth. 2007. When mussels die…an assessment of the mechanisms determining the upper limit of Mytilus californianus beds along the Pacific coast of North America. Western Society of Naturalists Annual Meeting, Ventura, CA. Steinbeck, J.R. 2010. Sh%t happens: how designing redundancy into a monitoring program can help exorcise intruding demons and increase the options for analysis and ability to detect change. . Southern California Academy of Sciences Annual Meeting, Los Angeles, CA. SWAT. 2008. Life in the tidepools and kelp forests. Seminar at Rancho del Oso Nature Center. *Tharratt, S. 2007. MARINe regional sampling update: offshore islands. MARINe Annual Workshop, San Francisco, CA. Thompson, S.A., K.J. Nielsen, C.A. Blanchette, B. Brockbank, and H.R. Knoll. 2007. Effects of commercial collection on growth and reproductive output of Postelsia palmaeformis. Ecological Society of America Annual Meeting, San Jose, CA. Thompson, S.A., K.J. Nielsen, C.A. Blanchette, B. Brockbank, and H.R. Knoll. 2007. The response of Postelsia palmaeformis to commercial collection across sites in California. Western Society of Naturalists, Ventura, CA. *Vogt, S., J.R. Smith, and S.N. Murray. 2010. Do native macro-invertebrates consume native over non- native seaweeds? Northwest Algal Symposium, Whidbey Island, WA. *Vogt, S.C., J.R. Smith, and S.N. Murray. 2010. The consumer’s dilemma, native or non-native seaweeds. Western Society of Naturalists Annual Meeting, San Diego, CA. *Vogt, S.C., L. Gilbane, A. Bullard, J.R. Smith, and S.N. Murray. 2007. Spatial and temporal variation in δ13C and δ15N values of macro-algae in southern California waters. Southern California Academy of Sciences Annual Meeting, Fullerton, CA. *Walters, K. 2009. Survey team monitoring summary: Mexico/Baja California. MARINe Annual Workshop, San Francisco, CA. *Walters, K. 2009. Today’s GPS: what it can do for you – a SWAT retrospective. MARINe Annual Workshop, San Francisco, CA. Waltz, G.T., J.R. Steinbeck, S.R. Kimura, and D.E. Wendt. 2007. Simulation of human activities and corresponding impacts to the temperate intertidal. Western Society of Naturalists, Ventura, CA. Waltz, G.T., S. Kimura, J.R. Steinbeck, and D.E. Wendt. 2009. Bare space or bountiful biota: an analysis of human disturbance on our rocky shoreline. Western Society of Naturalists Annual Meeting, Monterey, CA. *Weisberg, S.B. 2008. The subtle benefits of cooperative regional monitoring. MARINe Annual Workshop, San Pedro, CA. Whitaker, S. 2008. Experimental re-establishment of the rockweed Silvetia compressa at Little Corona del Mar. MARINe Annual Workshop, San Pedro, CA. Whitaker, S.G. and D.V. Richards. 2010. Widespread declines in abundances of rocky intertidal ecosystem modifiers and associated motile invertebrate species. Poster at Western Society of Naturalists Annual Meeting, San Diego, CA.

25 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

*Whitaker, S.G., J.R. Smith, and S.N. Murray. 2007. Experimental restoration of the rocky intertidal brown alga Silvetia compressa on urban southern California shores. Southern California Academy of Sciences Annual Meeting, Fullerton, CA. *Whiteside, K.E., J.R. Smith, and S.N. Murray. 2007. Distribution, habitat utilization, and reproductive patterns in Caulacanthus ustulatus (Caulacanthaceae, Gigartinales), a newly established seaweed on southern California shores. Southern California Academy of Sciences Annual Meeting, Fullerton, CA. *Worden, S. 2009. What is larval recruitment data telling us? MARINe Annual Workshop, San Francisco, CA.

Publications (2007-2010) Ambrose, R.F. 2008. Habitat restoration. Pp. 260-263. In: M.W. Denny and S.D. Gaines (eds.). Encyclopedia of Tidepools & Rocky Shores. University of California Press, Berkeley, CA. Becker, B.J., L.A. Levin, F.J. Fodrie, and P.A. McMillan. 2007. Complex larval connectivity patterns among marine invertebrate populations. Proceedings of the National Academy of Sciences 104:3267- 3272. Blanchette, C.A. and S.D. Gaines. 2007. Distribution, abundance, size and recruitment of the mussel, Mytilus californianus, across a major oceanographic and biogeographic boundary at Point Conception, California, USA. Journal of Experimental Marine Biology and Ecology 340:268-279. Blanchette, C.A., B. Helmuth, and S.D. Gaines. 2007. Spatial patterns of growth in the mussel, Mytilus californianus, across a major oceanographic and biogeographic boundary at Point Conception, California, USA. Journal of Experimental Marine Biology and Ecology 340:126-148. Blanchette, C.A., C.M. Miner, P.T. Raimondi, D. Lohse, K.E.K. Heady and B. Broitman. 2008. Biogeographic patterns of rocky intertidal communities along the Pacific coast of North America. Journal of Biogeography 35:1593-1607. Blanchette, C.A., D.R. Schiel, E.A. Wieters, B.R. Broitman, and B.P. Kinlan. 2009. Trophic structure and diversity in rocky intertidal upwelling ecosystems: A comparison of community patterns across California, Chile, South Africa and New Zealand. Progress in Oceanography 83:107-116. Blanchette, C.A., P.A. Raimondi and B.R. Broitman. 2009. Spatial patterns of intertidal community structure across the California Channel Islands and links to ocean temperature. Pages 161-173 In: Damiani, C.C. and D.K. Garcelon, (eds.), Proceedings of the 7th California Islands Symposium. Institute for Wildlife Studies: Arcata, CA. CD-ROM. *Broitman, B.R., C.A. Blanchette, B.A. Menge, J. Lubchenco, C. Krenz, M. Foley, P.T. Raimondi, D. Lohse and S.D. Gaines. 2008. Spatial and temporal patterns of invertebrate recruitment along the west coast of the United States. Ecological Monographs 78:403-421. Broitman, B.R., L. Szathmary, K.A.S. Mislan, C.A. Blanchette, and B. Helmuth. 2009. Predator-prey interactions under climate change: the importance of habitat vs. body temperature Oikos 118:219-224. *Conway-Cranos, L. 2009. Recovery dynamics in rocky intertidal communities: patterns, mechanisms, and simulations. Ph.D. Dissertation. University of California, Santa Cruz. *Del Sontro, T.S., I. Leifer, B.P Luyendyk and B.R Broitman. 2007. Beach tar accumulation, transport mechanisms, and sources of variability at Coal Oil Point, CA. Marine Pollution Bulletin 54:1461- 1471. Dethier, M.N. 2008. Monitoring: techniques. 2008. Pp.390-393. In: M.W. Denny and S.D. Gaines (eds.). Encyclopedia of Tidepools & Rocky Shores. University of California Press, Berkeley, CA.

26 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

Fenberg, P.B. and K. Roy. 2008. Ecological and evolutionary consequences of size-selective harvesting: how much do we know? Molecular Ecology 17:209-220. Hays, C.G. 2007. Adaptive phenotypic differentiation across the intertidal gradient in the alga Silvetia compressa. Ecology 88:149-157. *Helix, M.E., R.F. Ambrose, J.M. Engle, S.N. Murray, and P.T. Raimondi. 2007. Examining the health of rocky shores along the Pacific Coast – can local government and citizen’s help? Proceedings of Coastal Zone 2007 Symposium, Portland, OR. *Henkel, S. K., G. E. Hofmann, and A. C. Whitmer. 2007. Morphological and genetic variation in Egregia menziesii over a latitudinal gradient. Botanica Marina 50:159-170. *Henkel, S.K. and S.N. Murray. 2007. Reproduction and morphological variation in southern California populations of the lower intertidal kelp Egregia menziezii (Laminariales). Journal of Phycology 43:242-255. Huff, T.M. and J.K. Jarett. 2007. Sand addition alters the invertebrate community of intertidal coralline turf. Marine Ecology Progress Series 345:75-82. Hurtado L.A., M. Mateos, C.A. Santamaria. 2010. Phylogeography of supralittoral rocky intertidal Ligia isopods in the Pacific Region from Central California to Central Mexico. PLoS ONE 5(7): e11633. doi:10.1371/journal.pone.0011633. Lester, S.E., E.D. Tobin, and M.D. Behrens. 2007. Disease dynamics and the potential role of thermal stress in the sea urchin, Strongylocentrotus purpuratus. Canadian Journal of Fisheries and Aquatic Science 64: 314-323. Lester, S.E., S.D. Gaines, and B.P. Kinlan. 2007. Reproduction on the edge: large-scale patterns of individual performance in a marine invertebrate. Ecology 88:2229-2239. Lohse, D.P. and P.T. Raimondi. 2008. Barnacles. Pp. 61-64. In: M.W. Denny and S.D. Gaines (eds.). Encyclopedia of Tidepools & Rocky Shores. University of California Press, Berkeley, CA. Menge, B.A., M.M. Foley, J. Pamplin, G. Murphy, and C. Pemmington. 2010. Supply-side ecology, barnacle recruitment, and rocky intertidal community dynamics: Do settlement surface and limpet disturbance matter? Journal of Experimental Marine Biology and Ecology 392:160-175. Murray, S.N. 2008. Habitat alteration. Pp.256-260. In: M.W. Denny and S.D. Gaines (eds.). Encyclopedia of Tidepools & Rocky Shores. University of California Press, Berkeley, CA. Murray, S.N. 2008. Succession. Pp. 555-560. In: M.W. Denny and S.D. Gaines (eds.). Encyclopedia of Tidepools & Rocky Shores. University of California Press, Berkeley, CA. *Pfeiffer-Herbert, A.S., M.A. McManus, P.T. Raimondi, Y. Chao, and F. Chai. 2007. Dispersal of barnacle larvae along the central California coast: A modeling study. Limnology and Oceanography 52:1559- 1569. Phillips, N.E. 2007. A spatial gradient in the potential reproductive output of the sea mussel Mytilus californianus. Marine Biology 151:1543-1550. Phillips, N.E. 2007. High variability in egg size and energetic content among intertidal mussels. Biological Bulletin 212:12-19. Pister, B. 2007. Intertidal ecology of riprap jetties and breakwaters: marine communities inhabiting anthropogenic structures along the west coast of North America. Ph.D. Dissertation, UC San Diego. Raimondi, P., K. Cox, C. DaCosta, R. Gaddam, D. Lohse, C. Bell, M. George, M. Miner, and S. Worden. 2007. Reserves in reverse. In: PISCO Coastal Connections Vol 6. Partnership for Interdisciplinary Studies of Coastal Oceans.

27 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

*Raimondi, P., R. Sagarin, R. Ambrose, C. Bell, M. George, S. F. Lee, D. Lohse, C.M. Miner, and S.N. Murray. 2007. Consistent frequency of color morphs in the sea star Pisaster ochraceus (Echinodermata: Asteriidae) across open-coast habitats in the northeastern Pacific. Pacific Science 61:201-210. *Reed, D.C., S.J. Holbrook, C.A. Blanchette and S. Worcester. 2009. Patterns and sources of variation in flowering, seed supply, and seedling recruitment in surfgrass Phyllospadix torreyi. Marine Ecology Progress Series 384:97-106. Roy, K. 2008. Ecosystem changes, natural versus anthropogenic. Pp. 201-204. In: M.W. Denny and S.D. Gaines (eds.). Encyclopedia of Tidepools & Rocky Shores. University of California Press, Berkeley, CA. Sagarin, R. 2008. Climate change, overview. Pp. 137-140. In: M.W. Denny and S.D. Gaines (eds.). Encyclopedia of Tidepools & Rocky Shores. University of California Press, Berkeley, CA. *Sagarin, R.D., R.F. Ambrose, B.J. Becker, J.M. Engle, J. Kido, S.F. Lee, C. M. Miner, S.N. Murray, P.T. Raimondi, D.V. Richards, and C. Roe. 2007. Ecological impacts on the limpet Lottia gigantea populations: human pressure over a broad scale on island and mainland intertidal zones. Marine Biology 150:399-413. *Smith, J.R., P. Fong and R.F. Ambrose. 2009. “Spatial patterns in recruitment and growth of the mussel Mytilus californianus (Conrad) in southern and northern California, USA, two regions with differing oceanographic conditions.” Journal of Sea Research 61: 165-173. *Smith, J.R., P. Fong, and R.F. Ambrose. 2008. The impacts of human visitation on mussel bed communities along the California coast: are regulatory marine reserves effective in protecting these communities? Environmental Management 41:599-612. Thompson, S.A., H. Knoll, C.A. Blanchette and K.J. Nielsen. 2010. Population consequences of biomass loss due to commercial collection of the wild seaweed Postelsia palmaeformis. Marine Ecology Progress Series 413:17-31. *Whitaker, S., J.R. Smith, and S.N. Murray. 2010. Re-establishment of the southern California rocky intertidal brown alga, Silvetia compressa: an experimental investigation of techniques and abiotic and biotic factors that affect restoration success. Restoration Ecology 18:18-26.

Reports (2007-2010) *Ambrose, R.F. and N. Diaz. 2008. Pre-spill assessments of coastal habitat resources. Volume I: Development of protocols. California Department of Fish and Game Office of Spill Prevention and Response. 71p. *Ambrose, R.F. and N. Diaz. 2008. Pre-spill assessments of coastal habitat resources. Volume II: Quick response protocols. California Department of Fish and Game Office of Spill Prevention and Response. Ammann, K and P. Raimondi. 2008 Long-term monitoring protocol for rocky intertidal communities of Redwood National and State Parks, California. Natural Resource Report NPS/MWR/KLMN/NRR – 2008/034. National Park Service, Fort Collins, Colorado. Azimi-Gaylon, S., G. Lauenstein, D. Gregorio, and E. Siegel. 2008. Northern and Central California regional mussel survey draft work plan 2007-09. State Water Resources Control Board. 39p. *Conway-Cranos, T., P.T. Raimondi and R.F. Ambrose. 2007. Spatial and temporal variation in recruitment to rocky shores: relationship to recovery rates of intertidal communities. MMS OCS Study 2006-053. Coastal Research Center, Marine Science Institute, University of California, Santa Barbara, California. MMS Cooperative Agreement Number 14-35-0001-31063. 38 pages.

28 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

Cox, K. 2007. Abundance and distribution patterns of intertidal fishes at three sites within Redwood National and State Parks, 2004-2005. Thesis (M.S.)--Humboldt State University, Natural Resources: Fisheries Biology, 2007 Diehl, D., K. Maruya, J. Engle, D. Gregorio, R. Fay, and G. Lauenstein. 2007. 2007-08 Southern California regional mussel survey workplan. 42p. Kinyon, J., R. Gaddam, D. Schirokauer, R. Presiado, P. Raimondi. 2009. Coastal biophysical inventory database: Point Reyes National Seashore & Golden Gate National Recreation Area [Computer software]. Pacific Coast Science and Learning Center, National Park Service, Point Reyes Station, CA. Miller, K.A. 2007. Summary of nomenclatural and taxonomic changes for California seaweeds. University of California, Berkeley Herbarium. Miller, K.A. 2008. Summary of nomenclatural and taxonomic changes for California seaweeds. University of California, Berkeley Herbarium. Miller, K.A. 2009. Summary of nomenclatural and taxonomic changes for California seaweeds. University of California, Berkeley Herbarium. *Miner, M., B. Bealer, and L. Cooper. 2007. Revised MARINe Database User Guide. U.S. Minerals Management Service Report. 84 pages. Murray, S.N. and K.A. Miller. 2010. Marine macrophytes of the open-coast, rocky intertidal habitats of the Cabrillo National Monument. Final Report. Coastal Marine Ecology Laboratory, California State University, Fullerton. 56p. *Murray, S.N., P. Raimondi, and S.B. Weisberg. 2010. In pursuit of bio-criteria for evaluating the condition of rocky intertidal communities. Report of a workshop sponsored by the University of Southern California Sea Grant Program. with assistance from the Bureau of Ocean Energy Management, Regulation and Enforcement. 11p. National Park Service. 2008. North Coast and Cascades Network Intertidal Monitoring Protocol. Nelson PA, D Behrens, J Castle, G Crawford, RN Gaddam, SC Hackett, J Largier, DP Lohse, KL Mills, PT Raimondi, M Robart, WJ Sydeman, SA Thompson, S Woo. 2008. Developing wave energy in coastal California: potential socio-economic and environmental effects. California Energy Commission, PIER Energy-Related Environmental Research Program & California Ocean Protection Council CEC-500- 2008-083. Raimondi, P. 2008. Written summary of intertidal biological data for the Duxbury Reef Area of Special Biological Significance (ASBS), Bolinas, CA. Raimondi, P., D. Orr, C. Bell, M. George, S. Worden, M. Redfield, R. Gaddam, L. Anderson, and D. Lohse. 2009. Determination of the extent and type of injury to rocky intertidal algae and animals one year after the initial spill (Cosco Busan). A report prepared for OSPR (California Department of Fish and Game). Richards, D. V. and P. J. Rich. 2009. Rocky intertidal community monitoring, 2003 Annual Report. Natural Resource Technical Report NPS/CHIS/NRTR—2009/263. National Park Service, Fort Collins, CO. Richards, D. V. and P. J. Rich. 2010. Rocky intertidal community monitoring at Channel Islands National Park, 2005 Annual Report. Natural Resource Data Series NPS/CHIS/NRDS—2010/XXX. National Park Service, Fort Collins, Colorado. Richards, D. V. and S. G. Whitaker. 2010. Rocky intertidal community monitoring at Channel Islands National Park, 2009 Annual Report. Natural Resource Data Series NPS/CHIS/NRDS—2010/XXX. National Park Service, Fort Collins, Colorado.

29 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

Richards, D. V., and P. J. Rich. 2010. Rocky intertidal community monitoring at Channel Islands National Park: 2004 Annual Report. Natural Resource Data Series NPS/CHIS/NRDS—2010/064. National Park Service, Fort Collins, Colorado. Richards, D. V., D. Lerma, and P. Rich. 2010. Rocky intertidal community monitoring at Channel Islands National Park: 2002 Annual Report. Natural Resource Technical Report NPS/MEDN/NRTR— 2010/362. National Park Service, Fort Collins, Colorado. USC Sea Grant. 2009. Ship to shore: linking science to policy: loving the coast to depth. Article on Steve Murray’s Sea Grant rocky intertidal research. Urban Mariner 1 (2): October 2009. *VanBlaricom, G., M. Neuman, J. Butler, A. DeVogelaere, R. Gustafson, C. Mobley, D. Richards, S. Rumsey, and B. Taylor. 2009. Status review report for black abalone (Haliotis cracherodii Leach, 1814). Final report January 2009. NOAA Technical Memorandum NMFS-SWR-##. U.S. Department of Commerce, National Oceanic and Atmospheric Administration. National Marine Fisheries Service, Long Beach, CA.

Sample Data Requests (2010) *CSU Monterey Bay – Clover Lee Project: GIS predictive habitat model for black abalone Data Request: Black abalone habitat assessment data from 2007-2008

*UCSB – Stephen Gosnell Project: Modeling sea star density and distribution along the coast Data Request: Pisaster and Whelk density data at MARINe sites

UCSB – Carola Flores Fernandez Project: Integration of ecological, archaological, and paleoclimatic data in the study of past marine ecosystems Data Request: Shellfish abundance and mussel growth data for Channel Islands sites

*Duke University – Cliff Cunningham Project: Barnacle mortality as it relates to predator abundance and temperature Data Request: Site temperature data and Motile data, as well as general site information (bolt to bolts, maps, site summaries, tidal heights).

*MBNMS – Steve Lonhart Project: Determining areas where abalone may be present, for use in National Marine Sanctuary permitting process. Data Request: Lat/Longs and black abalone presence information at intertidal study sites between Pt Arena and Government Pt.

*University of South Carolina – Cristian Monaco Project: Interaction between Pisaster ochraceus and Mytilus californianus Data Request: All Pisaster and Mytilus density estimates, as well as Pisaster size data

30 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

ACKNOWLEDGEMENTS

This study would not have been possible without the assistance and understanding of the Project Technical Officer, Mary Elaine Helix.

We also could not have completed the work without a large number of volunteers who helped with field work, including Loana Addessi, Bengt Allen, Jessie Altstatt, Mike Ambrose, Monique Ambrose, Katherine Anderson, Araceli Anguiano, Katie Arkema, Joe Bayes, Mike Behrens, Sean Bergquist. Anne Boettcher, Helena Bowman, Debbie Boylen, Chris Bungener, Charlene Burge, Jennifer Burnaford, Tyra Byers, Don Canestro, Miranda Canestro, Jay Carroll, Jim Castle, Sarah Chaney, Henri Chomeau, Rachel Clausen, Lisa Conti, Garrett Cornish, Ann Dalkey, Kristin de Nesnera, Allyson Degrassi, Christian Degrassi, Stephanie Diaz, Rosylnn Dunn, Ginny Eckert, Chris Ehrler, Emily Engle, Shawn Erickson, Seri Feliciano, Nate Fletcher, Melissa Foley, Andrew Fredell, Victor Galvan, Anthony Garcia, Maya George, Amanda Gerrard, Bob Gladden, Constance Gramlich, Charlotte Greene, Mike Hearne, Scottie Henderson, Dave Hinrichs, Scott Holtz, Sarah Horwath, Dave Hubbard, Dania Huggins, Brittany Huntington, Zach Hymanson, Angela Johnson, George Johnson, Korie Johnson, Llad Johnson, Juli Kalman, Catherine Kaminski, Scott Kimura, Leah Kosareff, Julie Lancer, Shannon Leavey, Shannon Lee, Dave Lohse, Serena Lomonico, Maille Lyons, Laird MacDonald, James Marquez, Dan Martin, Amy McClean, Jamie McConnel, Greg McMichael, Mike Mitchell, Bobette Nelson, Jennifer O'Grady, Julie O'Neill, Dan Orr, Tamsen Peeples, Annalise Petriano, Rachel Piltz, Meredith Raith, Andrew Rice, Dan Richards, Mark Rigby, Jeff Rosaler, Ivan Sanchez, John Sayers, Andy Sharifi, Glenn Sias, Loretta Slusher, Ben Smith, Linda Smith, Lindsay Starrett, John Steinbeck, Jeanine Stier, Brianna Tarnower, Tetsuya Tsukamoto, Jeff Tupen, Carol Vandenberg, Amy Wagner, Kim Walker, Natalie Wenner, Kim Whiteside, Joe Wible, Demian Willette, and Amy Zimmer-Faust.

We would also like to thank Naomi Pleizier and Peter Shellenbarger for their help in the lab.

The BOEMRE intertidal team provided tremendous assistance in the field. This team consisted of: Ann Bull, Lisa Gilbane, Mary Elaine Helix, Dave Panzer, Fred Piltz, Greg Sanders, and Donna Schroeder.

We would like to thank Don and Miranda Canestro and the University of California Rancho Marino/Kenneth Norris Reserve for providing shelter from the elements and access to the reef. We gratefully acknowledge Hearst San Simeon State Park for access to Point Sierra Nevada and Vista del Mar, the Bureau of Land Management for access to Piedras Blancas, the Hearst Corporation for access to San Simeon Point, Harmony Headlands State Park for site access, Montaña de Oro State Park for access to Hazards, Hollister Ranch for access to Alegria, Carpinteria State Beach for site access, and Vandenberg Air Force Base for access to Boat House, Stairs, Purisima and Occulto. We would like to thank the Orange County Marine Protected Area Counsel and the Crystal Cove State Park for providing assistance and support for our work in Orange County; Cabrillo Marine Aquarium and the Friends of the Cabrillo Marine Aquarium for their support of the Point Fermin MARINe site and their support for the 2008 workshop; the Tatman Foundation (specifically, Jerry Chomeau, Henri Chomeau, and Chris Bungener) for their support of the sampling of the two Catalina Island sites (Bird Rock and Little Harbor); the Wrigley Marine Lab for supporting our field stays out there, and John and Robby Mazza and the Malibu Riviera Homeowner's Association for providing access to Paradise Cove.

31 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

LITERATURE CITED Abbott, I.A. and G.J. Hollenberg. 1976. Marine Algae of California. Stanford Univ. Press, Palo Alto, CA. Ambrose, R.F., D.C. Reed, J.M. Engle and M.F. Caswell. 1989. California comprehensive offshore resource study: summary of biological resources. Report to the California State Lands Commission. September 1989. 146 pp. Ambrose, R.F., K. Lafferty, J. Altstatt, C. Sandoval and P. Raimondi. 1993. Inventory of coastal wetlands in Santa Barbara County. Interim Report to the County of Santa Barbara. Ambrose, R.F., P.T. Raimondi and J.M. Engle. 1992a. Final study plan for inventory of intertidal resources in Santa Barbara County. Report to the Minerals Management Service, Pacific OCS Region. January 1992. 30 pp. plus appendices. Ambrose, R.F., P.T. Raimondi and J.M. Engle. 1992b. Proposed site locations and sampling protocol for inventory of subtidal resources in Santa Barbara County. Report to the Minerals Management Service, Pacific OCS Region. July 1992. 12 pp. Davis, G.E. 1985. Kelp forest monitoring program: a preliminary report on Biological sampling design. Univ. Calif. Davis Coop. National Park Resources Studies Unit. Tech. Rept. No. 19. 46 p. Davis, G.E. and J.M. Engle. 1991. Ecological condition and public use of the Cabrillo National Monument intertidal zone in 1990. U.S. National Park Service Resources Studies Unit. Tech. Rept. No. 20. 33 p. Engle, J.M., L. Gorodezky, K.D. Lafferty, R.F. Ambrose, and P.T. Raimondi. 1994. First year study plan for inventory of coastal ecological resources of the northern Channel Islands and Ventura/Los Angeles Counties. Report to the California Coastal Commission. September 1994. 31 p. Engle, JM. 2005. Unified Monitoring Protocols for the Multi-Agency Rocky Intertidal Network Foster, M. S., A. P. DeVogelaere, C. Harlod, J. S. Pearse, and A. B. Thum. 1986. Causes of spatial and temporal patterns in rocky intertidal communities of central and northern California. Outer Continental Shelf Study MMS 85-0049, Contract No. 14-12-0001-30057. Minerals Management Service, U.S. Department of the Interior. Kinnetic Laboratories, Inc. 1985. Field Survey Plan for successional and seasonal variation of the central and northern California rocky intertidal communities as related to natural and man-induced disturbances. Report to the Minerals Management Service. Littler, M.M., ed. 1979. The distribution, abundance, and community structure of rocky intertidal and tidepool biotas in the Southern California Bight. Southern California Baseline Study. Final Report, Vol. II, Rep. 1.0. U.S. Dept. of Interior, Bureau of Land Management, Washington, D.C. Littler, M.M., Littler D.S. 1979. Rocky Intertidal Island Survey. Vol. II, Report 5.0 in Southern California Intertidal Survey Year III. Prepared by Science Applications, Inc. for the Bureau of Land Management, Pacific OCS Office, Los Angeles, CA. Contract No. AA551-CT7-44. Littler, M.M., Littler D.S. 1980 California Mainland Rocky Intertidal Aerial Survey from Pt. Arguello to Pt. Loma, Prepared for the Bureau of Land Management, Pacific OCS Office, Los Angeles, CA. Murray, S.N. and M.M. Littler. 1981. Biogeographical analysis of intertidal macrophyte floras of southern California. J. Biogeography 8: 339-351. National Research Council. 1990a. Managing troubled waters: The role of marine environmental monitoring. National Academy Press, Washington, D.C. National Research Council. 1990b. Monitoring Southern California’s coastal waters. National Academy Press, Washington, D.C.

32 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

North, W.J., E.K. Anderson, and F.A. Chapman. 1989. Ecological Studies at Diablo Canyon Power Plant Final Report 1969-1987. Prepared for Pacific Gas & Electric. Raimondi, P.T., R.F. Ambrose, J.M. Engle, S.N. Murray and M. Wilson. 1999. Monitoring of rocky intertidal resources along the central and southern California mainland. 3-year report for San Luis Obispo, Santa Barbara and Orange Counties (Fall 1995 – Spring 1998). Technical Report. U.S. Department of Interior, Minerals Management Service, Pacific OCS Region (MMS Cooperative Agreement No. 14-35-0001-30761 with Southern California Educational Initiative, Marine Science Institute, University of California, Santa Barbara). Richards, D.V. and G.E. Davis. 1988. Rocky Intertidal Communities Monitoring Handbook. Channel Islands National Park, California. 15 pp. plus appendices. Tenera Environmental. 1988a. Diablo Canyon Power Plant Cooling Water Intake Structure, 316(b) Demonstration. Prepared for Pacific Gas & Electric. Tenera Environmental. 1988b. Diablo Canyon Power Plant Thermal Effects Monitoring Program. Final Report. Prepared for Pacific Gas & Electric. Tenera Environmental. 1994. Thermal Effects Monitoring Program. 1993 Annual Report. Diablo Canyon Power Plant. Prepared for Pacific Gas & Electric. Thompson, B., J. Dixon, S. Schroeter and D.J. Reish. 1993. Benthic Invertebrates. In: Dailey, M.D., D.J. Reish and J.W. Anderson, eds. Ecology of the Southern California Bight: A Synthesis and Interpretation. University of California Press, Berkeley, CA.

33 Multi-Agency Rocky Intertidal Network (MARINe) Study of Rocky Intertidal Communities Adjacent to OCS Activities – Final report (2007-2010)

APPENDIX

Selected Publications (attached) Henkel, S.K. and S.N. Murray. 2007. Reproduction and morphological variation in southern California populations of the lower intertidal kelp Egregia menziezii (Laminariales). Journal of Phycology 43:242-255 Murray, S.N., P. Raimondi, and S.B. Weisberg. 2010. In pursuit of bio-criteria for evaluating the condition of rocky intertidal communities. Report of a workshop sponsored by the University of Southern California Sea Grant Program. with assistance from the Bureau of Ocean Energy Management, Regulation and Enforcement. 11p. Raimondi, P., R. Sagarin, R. Ambrose, C. Bell, M. George, S. F. Lee, D. Lohse, C.M. Miner, and S.N. Murray. 2007. Consistent frequency of color morphs in the sea star Pisaster ochraceus (Echinodermata: Asteriidae) across open-coast habitats in the northeastern Pacific. Pacific Science 61:201-210. Smith, J.R., P. Fong and R.F. Ambrose. 2009. “Spatial patterns in recruitment and growth of the mussel Mytilus californianus (Conrad) in southern and northern California, USA, two regions with differing oceanographic conditions.” Journal of Sea Research 61: 165-173.

34 J. Phycol. 43, 242–255 (2007) r 2007 by the Phycological Society of America DOI: 10.1111/j.1529-8817.2007.00330.x

REPRODUCTION AND MORPHOLOGICAL VARIATION IN SOUTHERN CALIFORNIA POPULATIONS OF THE LOWER INTERTIDAL KELP EGREGIA MENZIESII (LAMINARIALES)1

Sarah K. Henkel2 Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, California 93106-9610, USA and Steven N. Murray Department of Biological Science, California State University, Fullerton, California 92834-6850, USA

Intertidal Egregia menziesii (Turner) Aresch. pop- the effect on turbulence (Koehl and Alberte 1988, ulations were studied at three Southern California Hurd and Stevens 1997, Hurd et al. 1997), mass trans- sites to determine temporal and spatial patterns of fer (Koehl and Alberte 1988, Hurd et al. 1996), and reproduction and morphology. The timing of spo- photon capture (Koehl and Alberte 1988, Wing and rophyll production and sporophyte recruitment was Patterson 1993, Wing et al. 1993). similar at all sites. Sporophyll production was much Egregia menziesii is one of the most variable and greater during winter periods of colder seawater complex of the kelps (Setchell 1893, Fritsch 1945), with temperatures and shorter day lengths. Sporophyte an adult morphology distinct from other species. Thal- recruitment occurred from spring through midsum- lus fronds can reach up to 15 m in length and consist of mer, ~5 months following maximal sporophyll pro- basal stipes that flatten to rachi as they become lined duction. Lateral blade morphologies varied in a with lateral blades and sporophylls (Setchell 1893, consistent manner, suggesting a developmental Setchell and Gardner 1925, Abbott and Hollenberg mechanism for form variation in Egregia thalli. 1976). Egregia is distributed from Alaska to Punta Spatulate blades dominated shorter axes and the Eugenio, Baja California, Me´xico, and grows intertid- bases of longer axes, whereas filiform laterals ally to depths of at least 20 m (Abbott and Hollenberg became abundant toward the tips of longer axes. 1976). The life history of Egregia is typical of members 1 1 Filiform laterals (9.8 mg O2 . g . h ) had higher of the order Laminariales, consisting of a microscopic light-saturated net photosynthetic rates than spatu- gametophyte and a conspicuous, perennial sporo- 1 1 late laterals (6.8 mg O2 . g . h ), resulting in a phyte. Zoospores produced in morphologically distinct 12% increase in the productivity of Egregia per sporophylls (Setchell 1893, Setchell and Gardner 1925, meter of filiform frond. Yoon et al. 2001) settle and germinate into gameto- Key index words: Egregia; herbivory; intertidal; phytes, which in turn produce eggs and sperm that kelp; morphology; photosynthesis; reproduction upon fertilization give rise to embryonic sporophytes (Myers 1928). Fertility of Egregia occurs from spring to fall in British Columbia (Gordon and De Wreede 1978) and presumably central California (Abbott and Kelps are conspicuous components of temperate Hollenberg 1976); sporophyte recruitment in South- seaweed communities in the eastern North Pacific ern California has been observed from January to June (North 1971, Foster and Schiel 1985), and these large (Black 1974, Murray and Littler 1977, Gunnill 1980, brown algae often exhibit species-specific variations in 1985). reproductive strategies (Reed et al. 1996) and morph- Egregia morphology varies considerably throughout ology (North 1971, Hurd 2000) in relation to environ- its range and is believed to correlate with geographic mental factors. Morphological variation, however, has distribution (Abbott and Hollenberg 1976, Blanchette been closely examined for few kelps, probably because et al. 2002). Historically, at least two and as many as of their large size and relative ease of identification. five species and subspecies of Egregia were recognized Previous research on internal and external thallus based largely on variations in the morphology of the morphology has focused mostly on the effects of rachis and lateral blades (Setchell and Gardner 1925, wave exposure (Parke 1948, Sundene 1962a, b, 1964, Silva 1957, Chapman 1962a). However, despite this Chapman 1973, Palmisano and Sheng 1977, Gerard high degree of morphological variation, currently only and Mann 1979, Gerard 1987, Roberson 2001) and one species (E. menziesii) and no subspecies of Egregia are recognized (Abbott and Hollenberg 1976). 1Received 21 March 2006. Accepted 8 January 2007. The lateral blades of Egregia can range from broad, 2Author for correspondence: e-mail [email protected]. ovate, or spatulate to highly dissected and filiform and

242 EGREGIA REPRODUCTION AND MORPHOLOGY 243 vary not only among thalli separated by many kilometers but also within local populations growing on the same or nearby shores (Chapman 1962a). Besides rep- resenting possible ecotypic variation, differences in lateral morphology may have ecological implications (Littler 1980, Littler and Littler 1980). For example, variations in lateral morphology may result in differences in thallus productivity (Odum et al. 1958, Chapman 1962b, Littler and Arnold 1982) and resist- ance to herbivory (Littler and Littler 1980; but see Padilla and Allen 2000). The purpose of this study was to determine the timing of reproduction and recruitment and to examine variations in thallus and lateral blade morphology in Egregia populations at three Southern California sites. Prior studies indicate that gametophyte fertility is reduced or inhibited at temperatures exceeding 161C (Myers 1928, Lu¨ning and Neushul 1978). Thus, we hypothesized that our Southern California populations of Egregia would produce fertile sporophylls mostly during fall and winter. Because the appearance of young Egregia thalli has been observed from late FIG. 1. Location of the three Southern California study sites: Crystal Cove, Shaw’s Cove, and Dana Point. spring to early summer (Black 1974, Murray and Littler 1977, Gunnill 1980, 1985), we hypothesized that peak recruitment of juvenile sporophytes would uplifted bedding planes. The study area was frequently inun- dated with sand, which at times covered Egregia holdfasts and be related to the fall and winter periods of sporophyll portions of stipes. The Shaw’s Cove sampling area was located production. Morphological plasticity is widespread in a surge channel; here, Egregia was observed growing on among seaweeds and often reflects environmental con- large, stable boulders and on channel sides below mussel beds. ditions (Dixon 1970, Hay 1981, Mathieson et al. 1981, Granitic boulders mixed with flattened benches characterized Lewis et al. 1987, Kilar and Hanisak 1989). Thus, we the Dana Point study site. Qualitative observations indicated also hypothesized that Egregia morphology would vary that grazing on Egregia was greatest at Shaw’s Cove where high densities of purple sea urchins [Strongylocentrotus purpuratus with differences in site conditions, such as wave expos- (Stimpson)] and kelp snails [Norrisia norrisi (Sowerby)] were ure or herbivory, and based on prior research (Chap- concentrated in the surge channel, where they were observed man 1962b, Littler and Littler 1980, Littler and Arnold feeding on Egregia. Strongylocentrotus purpuratus and occasion- 1982), we predicted that variations in Egregia lateral ally the red sea urchin S. franciscanus (Agassiz) and N. norrisi morphology would result in differences in thallus pro- were present but not abundant at Dana Point. Sea urchins were ductivity. not encountered in the immediate Crystal Cove study area, and kelp snails were rare. Recruitment and population structure. Recruitment of young Egregia sporophytes at each of the three sites was determined METHODS AND MATERIALS quarterly from January 2001 to February 2002. Results from Site descriptions. This research was conducted at three sampling performed during 2001 supported the prediction Southern California sites: Crystal Cove (33134.30 N, that Egregia sporophyte recruitment would occur during 117150.30 W), Shaw’s Cove (33132.80 N, 117148.20 W), and spring; consequently, in 2002, each site was sampled month- Dana Point (331270 N, 1171430 W), selected for their high in- ly from March to July to more precisely determine the mag- tertidal standing stocks of Egregia at the initiation of the study nitude and timing of sporophyte recruitment. Permanent (Fig. 1). These sites were distributed along an ~15.5 km section transect lines (10–12 m in length) were placed parallel to the of southwest facing coastline, which experiences moderate shore through Egregia populations at about Mean Lower wave exposure due to protection by the Channel Islands Low Water. At Crystal Cove and Dana Point, three bands (Ricketts et al. 1985, Hickey 1993). The average maximum were established perpendicular to transects during each site wave force was greatest at Dana Point (5.15 0.27 m s 1) visit using a random-number table. However, at Shaw’s Cove, followed by Crystal Cove (4.89 0.08 m s 1)andShaw’s the three bands were fixed and located where thalli were Cove (4.86 0.17 m s 1) based on data obtained in midshore most dense at the initiation of the study due to high topo- rockweed habitats during fall and winter of 1997 (Sapper and graphical heterogeneity and the patchy distribution of Murray 2003). Measurements taken throughout the year indi- Egregia in the surge channel. Each band was 1 m wide and cate that the three sites exhibit little site-to-site variation in daily 6 m long, resulting in six contiguous 1 m1 m plots that ex- sea temperature (11C) and salinity (1%). However, annual tended 3 m above and 3 m below the horizontal transect. sea temperatures in the region vary greatly by season and Within each plot, the number of Egregia sporophytes was re- ranged from 101Cto221C during the study (unpublished data corded and all Egregia thalli were assigned to one of four from Balboa reference station; Marine Life Research Group, (Types I–IV) developmental stages (Fig. 2). A Type I recruit Scripps Institution of Oceanography, La Jolla, CA). was defined as a laminarialean juvenile with a single, short The three study sites varied in substratum topography and blade. With the exception of only the smallest juvenile spo- herbivore pressure. At Crystal Cove, flattened and angled rophytes (<4cm in length), Type I Egregia recruits could be benches were separated by shallow channels located between distinguished from Eisenia arborea Aresch. recruits because 244 SARAH K. HENKEL AND STEVEN N. MURRAY

0.5 m

5 cm 1 cm

Type I Type II Type III Type IV

FIG. 2. Developmental stages of Egregia sporophytes. Type I: short stipe and single blade. Type II: single blade with marginal leaﬂets. Type III: short branching thallus with well-developed rachi (<25cm), <3 pneumatocysts, and terminal blades deteriorating. Type IV: Differentiated, mature sporophyte. Scale bar, 0.5 m for stages III and IV.

Egregia juveniles had smooth blades, whereas E. arborea ulations were haphazardly selected, and the first axis of each juveniles had wrinkled or corrugated blades. No other kelps thallus with an intact meristem and a length 450 cm was ex- were observed to recruit into intertidal habitats at our sites cised and taken to the laboratory. Each axis was divided into during the study. Type II Egregia juveniles had a single blade five 5 cm sections such that 5 cm located just below the mer- with marginal leaflets. Type III (subadult) was defined as a istem was sampled, 5 cm just above the base of the axis was short (25 cm) branching thallus with a well-developed ra- sampled, and the three remaining 5 cm sections were evenly chis and less than three pneumatocysts. Type IV was a ma- dispersed between the apical and basal sections. Vegetative ture, differentiated Egregia thallus possessing more than one lateral blades and sporophylls were counted in each section. axis and more than three pneumatocysts. Vegetative laterals were assigned to one of three morphs (fil- Morphological features of mature Egregia thalli were deter- iform, spatulate, or intermediate; Fig. 3) to characterize pat- mined at the three sites. The nearest Type IV Egregia thallus terns of lateral morphology; the percentage of each morph within a 0.5 m radius of each 1.0 m mark along each transect was determined relative to axis location for each sampled was identified to generate a sample size of 12–22 individuals thallus. per site visit. The longest axis of each thallus was measured Reproductive periodicity was determined by the density of from holdfast to tip, and the total number of axes was counted. sporophylls along the same axis sections. To ensure that the The numbers of viable (with meristem) and nonviable (sans sporophylls counted were fertile, one axis from each site was meristem) axes also were determined. randomly selected each month that axes with sporophylls were Sporophyll production and lateral morphologies. Patterns of collected. Five sporophylls were then haphazardly excised and Egregia sporophyll production and lateral blade morphology sectioned to check microscopically for the presence of mature at each site were determined monthly from February 2001 to sporangia. The amount of biomass allocated to sporophyll pro- February 2002. Nine thalli growing adjacent to sampled pop- duction was also estimated for each Egregia axis. Subsamples of EGREGIA REPRODUCTION AND MORPHOLOGY 245

tions, thallus parts were returned to the laboratory and dried to constant weight at 601C. Light (318–974 mmol photons m 2 s 1) and temperature (15–191C) varied among experiments; however, analyses failed to show statistically significant differences in net photosynthetic and dark respi- A. Filiform ration rates among experiments performed on different days and under the range of temperature and light conditions employed. Hence, data from all sampling dates were pooled for analysis. Photosynthetic rates are believed to represent light-saturated values based on reports of requirements for saturating intertidal seaweeds (300–1200 mmol photons m 2 s 1;Lu¨ning 1981). Statistical analyses. Each data set was examined for variance homogeneity using Cochran’s and Levene’s tests and B. Spatulate transformed if necessary to meet parametric requirements. A one-wayanalysisofvariance(ANOVA)wasusedtotestthe hypothesis that photosynthetic and dark respiration rates differed among thallus parts. Where differences were significant, Student–Newman–Keuls’ multiple comparison tests were used to differentiate subsets of means to facilitate interpretation of ANOVA results. Two-way ANOVA models were employed to analyze the effects of the fixed factors site and sampling period on the numbers of sporophylls, numbers of different lateral morphs, maximum axis length, C. Intermediate and the percentage of viable axes. Variance criteria were met either by the original data or following transformation in all analyses. 2 cm The nonparametric Spearman’s rank correlation procedure was used to determine whether a statistical relation- FIG. 3. Vegetative lateral types used in morphological ana- ship could be detected between seasonal patterns of sporo- lyses of Egregia axes. phyll production and seawater temperatures or photoperiods. Surface seawater temperatures (SSTs) used in this analysis were obtained from the Balboa, Newport Beach, CA, sporophylls, each lateral morph, and sections of the rachis reference station (Marine Life Research Group, Scripps Insti- were dried to constant weight at 601C. The percentage tution of Oceanography; unpublished data), whereas hours of Egregia biomass allocated to sporophylls was determined of daylight were calculated from sunrise and sunset data using the mean dry weights (dwt) of these subsamples reported in National Oceanographic and Atmospheric Associ- and their abundances, and the dwt to length relationship for ation (NOAA) tide tables for outer Newport Bay (Anonymous the rachis. 1998). Herbivore densities. The primary benthic herbivores observed feeding on Egregia at the three sites included Strong- ylocentrotus spp. (urchins); N. norrisi (kelp snail); and RESULTS Notoacmaea insessa (Hinds), a limpet that lives and feeds on the Egregia rachis (Black 1976). In order to quantify differ- Sporophyll production. The morphology of Egregia ences in herbivore abundances, and presumably grazing sporophylls varied depending on the form of the as- pressure, among the three sites, the numbers of red and sociated vegetative laterals. Sporophylls associated purple urchins and kelp snails in each plot were determined, with filiform laterals were thick, strongly furrowed, and the number of N. insessa on each measured Type IV and raisin-like in appearance, with filiform exten- Egregia thallus was recorded. sions often seen growing from sporophyll termini. In Photosynthesis experiments. Photosynthetic rates of different contrast, sporophylls produced in spatulate regions parts of Egregia thalli were determined in the field at Dana Point, California, on March 11, and April 4 and 16, 2002, of the axis were flattened, with plump and wrinkled following methods similar to those described by Littler and basal portions (Fig. 4). Microscopic examination re- Arnold (1980, 1985). Spatulate blades, filiform laterals, in- vealed that almost all examined sporophylls had fer- termediate laterals, sporophylls, and bare rachi without ep- tile sori and that fertile sori could be detected year- iphytes were excised from freshly collected Egregia thalli and round(Table1).Thegreatestproportionofexam- submerged in trays for 1–2 h before incubation. Four to six ined sporophylls were fertile during winter. Sporo- replicates of each thallus part were then incubated in filtered (10 mm) seawater for 10.5 h (light treatments) or 20.5 h phylls with mature sporangia tended to be darker (dark treatments) within closed 0.5 L French square glass and more wrinkled but were of similar thickness as bottles. During incubations, bottles were kept submerged in nonfertile sporophylls. shallow plastic trays, which were replenished with seawater Sporophyll production varied greatly over time every 10–15 min to maintain ambient seawater temperature. (F11, 286 5 16.593, P<0.001) but did not vary among Incubation bottles were thoroughly mixed every 5–10 min sites (F 5 2.475, P 5 0.08; two-way ANOVA); a using magnetic stirrers to break down diffusion barriers. 2, 286 Changes in dissolved oxygen (DO) concentration were meas- significant interaction between time and sites was ured with Yellow Springs Instrumentst oxygen electrodes not detected (F22, 286 5 1.528, P 5 0.06), suggesting (Yellow Springs, OH, USA) and used to calculate net that the seasonal patterns of sporophyll production photosynthetic and dark respiration rates. Following incuba- were similar at the three sites (Fig. 5). Sporophyll 246 SARAH K. HENKEL AND STEVEN N. MURRAY

20 16 Temperature A 18 Hours of Daylight 14 C ° 16

14 12

Temperature 10 10 Number of Daylight Hours 10

1 9 Shaw's Cove B − Crystal Cove 8 Dana Point 7 6 5 4 3 2

FIG. 4. Variable sporophyll morphologies. (A) Filiform spor- Number of Sporophylls cm 1 ophylls. (B) Spatulate sporophylls. 14 12 C production was much greater in December and 10 January, during periods of colder mean monthly 8 ocean temperatures (11–131C) and shortest daylight 6 hours (9.9–10.5 h), and least during the periods Biomass 4 of warmer sea temperatures (17–191C) and longer days (12.5–14.5 h). Sporophyll densities exhibited 2 Sporophyll % of Thallus significant negative correlations with both sea tempera- 0 ture (r 5 0.50; P 5 0.02) and hours of daylight F MAMJ J ASOND J F 2001 2002 (r 5 0.81; P<0.001). At all sites, densities of Egregia 1 sporophylls were high (3.1–3.8 cm axis ) at the ini- FIG. 5. (A) Surface seawater temperatures and hours of day- tiation of the study in winter 2001 and then dropped to light during the study period (monthly means). (B) Patterns of nearly zero by spring. The number of sporophylls var- sporophyll production in Egregia menziesii populations from the ied greatly among thalli but remained low for most of three study sites. Values are monthly means (1 SE) of spor- 1 ophyll numbers per cm of axis for nine replicates from each site. the summer before peaking again (5.0–7.9 cm axis ) (C) Mean (þ1 SE) percentage of dry biomass allocated to the next winter between November and January. Al- sporophylls based on pooled samples from all three sites (see though variable among sites, small, short-lived increas- Methods and Materials for calculation). es in summer sporophyll production appeared to follow periods when ocean temperatures at the Bal- boa reference station dropped for a few days to 131C. across sites, ranged from a low of 0.6% in July 2001 to a The amount of total biomass (above the holdfast) allo- high of 14.9% in January 2002, the period of greatest cated to sporophyll production showed a seasonal pat- sporophyll production (Fig. 5). tern similar to sporophyll densities. The percentage of Sporophyte recruitment. Recruitment of juvenile dry biomass allocated to reproductive tissues, pooled sporophytes showed similar patterns at all sites

TABLE 1. Sporophyll fertility.

2001 2002

April May June July August September October November December January February Shaw’s Cove 5 – 2 – 3 3 4 5 5 5 5 Crystal Cove 0 3 4 – – 5 2 2 5 5 5 Dana Point – 0 5 – – 0 3 3 3 5 5 Mean (%) of fertile sporophylls 50 30 70 0 60 53 60 67 87 100 100

Reported are the monthly numbers of sporophylls with mature sporangial sori based on microscopic examination of sections of ﬁve sporophylls from each site (n 5 5). Dashes indicate month-site combinations where no sporophylls were present on examined Egregia axes. EGREGIA REPRODUCTION AND MORPHOLOGY 247

FIG. 6. Seasonal abundances of Egregia sporophytes by developmental stage. Plotted are the mean densities (1 SE) of the four developmental stages (Types I–IV) for the three study sites. Mean values are based on ﬁeld surveys of plots (n 5 18) distributed along transect lines. and between years (Fig. 6), although the intensity (adult) Egregia thalli varied significantly among sites of recruitment varied greatly among sites and years. but not over time, and a significant interaction You ng (Ty pe I ) Egregia sporophytes showed peak between site and season was not detected densities ~5 months following the period of greatest (Table 2). The average number of axes per Type IV sporophyll production at all sites. Type I thalli thallus was greatest at Shaw’s Cove (16.61.5) and appeared in March 2001, were found at all sites leastatCrystalCove(9.50.8). The percentage of through July or August, and then were almost axes with viable meristems also differed significantly completely absent by the ensuing fall and winter. among sites and seasons, and a significant interaction This pattern was repeated the next year when between site and season was observed (Table 2). Des- recruits again became abundant in March 2002 pite having more axes per Type IV thallus, Egregia and persisted through July. During 2002, maxi- from Shaw’s Cove had the lowest average percentage mum Type I sporophyte recruitment occurred of axes with intact meristems compared with thalli at at Dana Point in March (35.7 m 2) followed by Shaw’s Dana Point or Crystal Cove. As supported by the sig- Cove in April (5.9 m 2)andCrystalCovein nificant interaction, thepercentageofviableaxes May (1.8 m 2). (with meristems) increased at Shaw’s Cove from Adult sporophyte morphology and herbivore densities. The July through December but dropped at Dana Point number of axes in ﬁeld populations of Type IV duringthesameperiod. 248 SARAH K. HENKEL AND STEVEN N. MURRAY

TABLE 2. Number of axes and percentage of axes with viable meristems for Type IV Egregia sporophytes.

Sampling period

Site January–February April–June July–September October–December Number of axes Crystal Cove 9.3 1.6 8.5 1.4 11.4 1.9 8.8 1.1 Shaw’s Cove 14.0 1.6 13.1 3.0 13.2 3.4 21.5 4.0 Dana Point 12.4 2.0 15.4 2.0 14.9 2.1 11.7 1.9

Two-way ANOVA df MS FP

Site 2 0.436 6.132 0.003** Season 3 0.030 0.420 0.743 ns Site season 6 0.133 1.871 0.087 ns % Viable axes Crystal Cove 47.5 3.9 61.0 7.3 51.5 5.7 50.5 6.7 Shaw’s Cove 33.1 3.7 39.0 7.2 61.1 5.3 42.7 5.0 Dana Point 50.4 4.7 64.9 4.6 49.7 5.1 36.4 5.6

Two-way ANOVA df MS FP

Site 2 0.177 3.274 0.039* Season 3 0.213 3.930 0.009** Site season 6 0.174 3.211 0.005** **P<0.01; *P<0.05; ns, not significant (P0.05). Reported are mean values (1 SE) for each of the three study sites based on 12–22 replicates for the indicated sampling periods. Values for axis numbers were log 10 transformed before analysis of variance (ANOVA).

TABLE 3. Maximum axis lengths for Type IV Egregia sporophytes.

Site January–February April–June July–September October–December Crystal Cove 2.53 0.35 2.76 0.35 2.72 0.26 1.34 0.19 Shaw’s Cove 0.39 0.04 0.37 0.03 0.55 0.04 0.50 0.05 Dana Point 1.43 0.15 1.42 0.14 1.92 0.23 1.58 0.13

Two-way ANOVA df MS FP

Site 2 50.020 192.376 <<0.001*** Season 3 1.532 5.891 <0.001*** Site season 6 0.750 2.885 0.010** ***P<0.001; **P<0.01; ns, not significant (P0.05). Reported are mean values (1 SE) based on 12–22 replicates for each of the three study sites for the indicated sampling periods. Annual mean is calculated as the grand mean of the four period means. Analysis by two-way analysis of variance (ANOVA) with site and season as ﬁxed factors. Values for axis lengths were transformed using the Box-Cox procedure before ANOVA.

Maximum axis lengths varied significantly among thalli and with the lowest percentage of viable axes. sites and seasons, and a significant interaction was Densities of these herbivores were much lower at Dana found between these ﬁxed factors (Table 3). Egregia Point, where purple urchins (1.50.7 m 2) and kelp thalli were much shorter at Shaw’s Cove throughout snails (<0.1<0.1 m 2) were uncommon, and at the year (mean 5 0.45 m0.02 m) than thalli collected Crystal Cove, where kelp snails were rare from Dana Point (mean 5 1.57 m0.07 m) and Crystal (<0.1<0.1 m 2) and urchins absent from the imme- Cove (mean 5 2.42 m0.16 m). Maximum axis lengths diate study area. Numbers of N. insessa inhabiting Eg- were more varied at Crystal Cove and, unlike thalli at regia thalli also varied among sites (Table 4). Much Shaw’s Cove and Dana Point, were much shorter dur- higher numbers of N. insessa per Egregia axis, as well as ing October to December than previous seasons at the densities (number per axis cm 1), were found at Crys- conclusion of the study. tal Cove compared with the other two sites. As expected, densities of N. norrisi and Strongyl- Patterns of lateral morphology. The percentages of ocentrotus spp. varied among sites (Table 4). Purple spatulate laterals varied significantly by site 2 2 urchin (51.8 3.9 m ) and kelp snail (2.2 0.2 m ) (F2, 285 5 109.8, P<0.001) but not by season densities were much greater at Shaw’s Cove, the site (F11, 285 5 1.6, P 5 0.10), and an interaction between with the shortest and more-profusely branched Egregia siteandseasonwasnotdetected(F22, 285 5 1.3, EGREGIA REPRODUCTION AND MORPHOLOGY 249

TABLE 4. Herbivore densities.

Crystal Cove Shaw’s Cove Dana Point Strongylocentrotus pupuratus Stimpson, 1857 0 51.8 3.9 1.5 0.7 Strongylocentrotus franciscanus A. Agassiz, 1863 0 0.1 <0.1 < 0.1 <0.1 Norrisia norrisi Sowerby, 1938 < 0.1 <0.1 2.2 0.2 < 0.1 <0.1 Notoacmaea insessa Hinds, 1842 2.3 0.9 < 0.1 <0.1 0.7 0.3

Reported are mean densities (number m 2) 1 SE of urchins (Strongylocentrotus sp.) and kelp snails (Norrisia norrisi) for the three study sites based on averages over all monthly site visits (n 5 9–10). Reported for Notoacmaea insessa are the number of individuals per Egregia axis averaged over all monthly collections (n 5 90–103 per site).

P 5 0.13; Fig. 7a). The percentage of filiform laterals laterals were more prevalent basally, with intermedi- similarly varied significantly by site (F2, 286 5 ate laterals becoming more common on longer axes. 122.8, P<0.001) and additionally varied by season Finally, filiform laterals became increasingly abun- (F11, 286 5 3.6, P<0.001), declining in winter during dant with axis length and were most profuse apically. the period of greatest sporophyll production; again, Thus, shorter axes had predominately spatulate lat- aninteractionbetweensiteandseasonwas erals, and longer axes bore higher numbers of inter- not found (F22, 286 5 1.2, P 5 0.24; Fig. 7b). Spatulate mediate and filiform laterals.

FIG. 7. Monthly patterns of Egregia lateral morphology at three sites. Values are the percentage (1 SE) of spatulate (A) or ﬁliform (B) of the total identiﬁable vegetative laterals for the indicated sampling periods. 250 SARAH K. HENKEL AND STEVEN N. MURRAY

FIG. 9. Light-saturated net photosynthesis and dark respiration rates for Egregia thallus parts. Plotted are means (þ1SE) based on 9–12 replicates. Letters represent statistically signiﬁcant subsets of means based of Student-Newman-Keuls’ test results.

of the other lateral types. Intermediate (7.6 1 1 0.1 mg O2 g h ) and spatulate (6.80.1 mg O2 g 1 h 1) laterals formed a subset with statistically indistinguishable rates, which were greater than the rates exhibited by the sporophylls (2.90.1 mg O2 1 1 1 1 g h ). The rachis (0.8<0.1 mg O2 g h ) had the lowest photosynthetic rate of any incubated thallus part. Dark respiration rates also differed signif- FIG. 8. Lateral morphology by axis position. (A) Shaw’s Cove. icantly among thallus parts (Fig. 9). Among vegetative (B) Dana Point. (C) Crystal Cove. Plotted are percentages (þ1 SE) laterals, dark respiration rates of the filiform of identifiable vegetative laterals for filiform, spatulate, and 1 1 (1.2 0.1 mg O2 g h ) and intermediate (1.1 intermediate morphs by axis location based on the indicated 1 1 number of sampled thalli. Axis positions (A–E) are defined in the 0.1 mg O2 g h ) laterals were highest and statisti- Methods and Materials and represent a gradient from the cally indistinguishable. Intermediate rates of respiration meristem (A) to the basal (E) part of the axis. were observed for the sporophylls (0.9 0.1 mg 1 1 O2 g h ), and the lowest rates were found for 1 1 spatulate laterals (0.50.1 mg O2 g h )andthe 1 1 At Shaw’s Cove, where the axes collected for mor- rachis (0.4<0.1 mg O2 g h ). phological analysis were shortest (0.66 0.02 m), thalli almost exclusively produced spatulate laterals and generally bore only a few intermediate laterals, which DISCUSSION were located mostly near growing meristematic tips Southern California populations of E. menziesii, like (Fig. 8a). At Dana Point, where axes of intermediate many perennial macroalgae occurring outside the length (1.140.05 m) were collected, intermediate and tropics, exhibited a strong seasonal pattern of repro- filiform laterals were found in the highest duction. These results are consistent with previous re- percentages at the distal ends near the meristems; ports (Abbott and Hollenberg 1976, Gordon and most axes, however, possessed spatulate laterals, De Wreede 1978) of seasonal peaks in Egregia fertility. particularly at their basal regions (Fig. 8b). Filiform Similar to Egregia from Santa Barbara (Black 1974, laterals dominated the upper (distal) half of the longer 1976), the Southern California Egregia populations in axes (1.290.05 m) collected from Crystal Cove; but, this study showed greatest sporophyll production and as was the case at both Shaw’s Cove and Dana Point, sorus fertility from December through February, when basal portions of axes retained mostly spatulate laterals monthly SSTs averaged 11–131C. Similar results were (Fig. 8c). observed for Egregia from British Columbia (Gordon Photosynthesis and respiration. Rates of net photosyn- and De Wreede 1978), where summer temperatures of thesis and dark respiration varied significantly among 10 and 151C coincided with greatest production of Egregia thallus parts (F4, 49 5 63.8, Ppsn<0.001; F4, 49 5 gametophytes and sporophytes, and winter tempera- 16.4, Presp<0.001; Fig. 9). As hypothesized, filiform tures of 71C depressed gametophyte and sporophyte laterals had significantly higher light-saturated net pho- development. Furthermore, Myers (1928) found that 1 1 tosynthetic rates (9.8 0.1 mg O2 g h ) than any the male gametophytes would not release their an- EGREGIA REPRODUCTION AND MORPHOLOGY 251 therozooids at temperatures of 161C or greater. Other shorter days and coldest ocean temperatures (Fig. 5). reports (Abbott and Hollenberg 1976) indicate that in Other studies also provide support for a cold tempera- California, Egregia produces sporophylls between April ture requirement for successful Egregia reproduction. and November. Although we observed much greater Spores released from Egregia collected in northern fertile sporophyll production during winter, small California in the fall and cultured under conditions numbers of sporophylls, some of which were fertile, of 10–181C produced gametophytes and completed were detected throughout the year, reinforcing the the life history by giving rise to new sporophytes in suggestion (Abbott and Hollenberg 1976) that Egregia 19–28 days (Myers 1928). In contrast, material collect- can be reproductive year-round. We did not investi- ed in summer and cultured under warmer ambient gate the roles of spore production and germination temperatures (16–201C) produced gametophytes but success, however, and seasonal differences in these pa- failed to give rise to new sporophytes (Myers 1928). rameters could significantly affect the reproductive Moreover, the optimum temperature for the onset of patterns derived soley from sporophyll production. gametophyte fertility in Southern California Egregia is With this qualification, the reproductive pattern ob- 121C, and gametophyte fertility was inhibited at 201C served for Egregia in this study appears to be similar to (Lu¨ning and Neushul 1978). that observed for Macrocystis pyrifera (L.) C. Agardh As expected for algae (Hoffmann and Santelices (Neushul 1963, Anderson and North 1967, Reed et al. 1991), especially species with distinct gametophyte and 1996) and Laminaria saccharina (L.) Lamour. (Druehl sporophyte stages, we observed a lag between the and Hsiao 1977, Lee and Brinkhuis 1986), species period of greatest fertile sporophyll production by which also show seasonal peaks in spore production Egregia and the detection of new sporophyte recruits but can be reproductive year-round. Unlike Southern in the spring. We measured the greatest recruitment California populations of Egregia, however, both M. of juvenile Egregia sporophytes from March through pyrifera and L. saccharina exhibit a second peak in spore June, 5 months following the time of maximum production during the year, with spore germination sporophyll and, presumably, spore production. This success varying greatly between the two periods (De- peak was similar to the spring maxima in Egregia ysher and Dean 1986). The single, strong reproductive sporophyte recruitment reported for other Southern period found in Egregia also resembles the narrow re- California sites, including La Jolla (Gunnill 1980, productive window observed in Pterygophora californica 1985) and San Clemente Island (Murray and Littler Rupr., although this kelp produces spores only from 1977, 1978), but later than that observed in Santa November through April regardless of environmental Barbara, California, where new sporophyte genera- conditions (Reed et al. 1996). tions recruited from January to March (Black 1974, Reproductive effort can be determined by measur- 1976). ing the proportion of thallus biomass allocated to re- Intertidal populations of Egregia exhibit a life histo- productive tissues (Chapman 1985); however, such ry strategy in Southern California that appears to be calculations are difficult to perform and must be inter- timed to coincide with optimal conditions for repro- preted with caution in kelps and other seaweeds where ductive success. Egregia produces sporophylls and re- many very small reproductive cells are produced in leases its spores following the summer period of sori (Santelices 1990). Nevertheless, the amount and greatest growth (Black 1974) and during stressful win- seasonal pattern of biomass allocated to reproductive ter periods when the lower of the mixed semidiurnal tissue in Egregia (14.9% of dwt in January to 0.6% in low tides occurs in the afternoon (Seapy and Hoppe July) were similar to reports (Novaczek 1984) for 1973, Seapy and Littler 1982, Littler et al. 1991). Ecklonia radiata (C. Ag.) J. Ag. (17% frond surface Hypothetically, the few-celled gametophytes produced area covered with sori in winter to 0.2% in summer), during this period are able to develop in microhabitats another member of the Alariaceae. Our values, how- protected from desiccation under the cold water ever, are higher than those reported for M. pyrifera temperatures required for optimizing fertility (Myers (4%; Neushul 1963) and lower than reports for 1928, Lu¨ning and Neushul 1978). The spring recruit- Laminaria sp. (2%–30%; Kain 1971, 1975, Perez 1971, ment of vulnerable juvenile sporophytes takes place DeWreede and Klinger 1988), Ascophyllum nodosum (L.) later in the year when the timing of lower tides shifts Le Jol. (40%–60%; Cousens 1986), and other fucoids toward the early morning, and lower shore habitats (80%–90% of the deciduous fronds; Santelices 1990). It occupied by Egregia are emersed for only brief periods is unlikely that the winter peak in the proportion (Seapy and Hoppe 1973, Littler et al. 1991). Spring of reproductive biomass observed for Southern recruits of Egregia at the three sites appeared to California Egregia populations is due to winter biomass reach reproductive maturity in 6–7 months, as evi- loss (as has been reported for Macrocystis; Graham denced by observations during the fall of sporophylls 2002, 2003) because minimum axis lengths were found present on young, newly recruited thalli <50 cm in the spring at two of the three sites, and there was no in length. Reproduction in the first season is common significant difference among seasons for the number of in intertidal kelps because, although they are potential axes per thallus. perennials, the vast majority behave as annuals Maximum sporophyll production in our Egregia under stressful intertidal conditions (Druehl and Hsiao populations occurred during winter conditions of 1977). 252 SARAH K. HENKEL AND STEVEN N. MURRAY

The highly seasonal winter peak in sporophyll narrow leaflets that develop proliferations or that with production and spring peak in sporophyte recruit- increasing age broader blades become eroded and ment suggest that reproductive success in intertidal proliferated. However, we observed that filiform later- Egregia is influenced by environmental conditions als developed directly on the distal ends of longer axes, during these critical periods. For example, abnormal- a finding that contradicts Chapman’s hypotheses. ly warm, winter ocean temperatures might reduce Chapman (1962a) additionally reported that shallow, Egregia sporophyll production and gametophyte fer- wave-exposed forms of Egregia with short thalli had tility. Moreover, algal propagules and early postsettle- axes covered with broad laterals and hypothesized that ment stages are known to experience high mortality the shorter life span of these smaller, heavily buffeted under a variety of abiotic and biotic conditions (Vadas individuals prevented complete erosion of the leaflets. et al. 1992), and kelp gametophytes and microsporo- Alternatively, we attribute this dominance of broad, phytes are highly vulnerable to burial and scour by spatulate laterals on shorter Egregia axes to develop- sediments (Neushul et al. 1976, DeVinny and Volse mental patterns and not to the absence of blade ero- 1978, Dayton et al. 1984) and to grazing pressure sion. (Kain and Jones 1966). The large discrepancy between The form of an algal thallus is known to correlate the high number of fertile Egregia thalli and the ensu- with nutrient-uptake abilities (Odum et al. 1958), pho- ing small number of young sporophyte recruits sug- tosynthetic and respiration rates (Kanwisher 1966, Lit- gests that postsettlement survival of gametophytes and tler and Murray 1974, King and Schramm 1976, young sporophytes is crucial to maintaining Egregia Littler 1980, Littler and Littler 1980, Littler and populations at our study sites. Arnold 1982), and possibly susceptibility to herbivory Our studies are the first to demonstrate that varia- (Littler and Littler 1980, but see Padilla and Allen tions in lateral morphology can be related to axis 2000). Differences in photosynthetic and respiration length and provide a possible mechanism for the rates for different stages of development and different development of different lateral morphologies on the parts of Egregia thalli have been reported previously. same Egregia thallus. Variations in the morphology of For example, whole, young Egregia thalli had net pho- Egregia laterals have long been recognized (Setchell tosynthetic rates that were ~2.5 times the rates of fully 1893) and were previously used as a basis for discrim- differentiated adult thalli (Littler and Littler 1980, inating species and varieties within the genus Littler and Arnold 1982). Similarly, variations in (Chapman 1962a). Lateral morphologies in Egregia photosynthesis to respiration ratios (Clendenning show strong geographic patterns: both broad, spatu- and Sargent 1958) and in net photosynthetic rates late, and narrow, filiform laterals occur on Southern (Druehl 1984) have been observed for different California thalli (Abbott and Hollenberg 1976), where- thallus parts in Macrocystis. as narrower and thicker spatulate laterals commonly The results of the photosynthesis experiments sup- occur north of Point Conception, California (Blanche- ported earlier studies conducted by Chapman (1962b) tte et al. 2002). Results for our Southern California and confirmed that net photosynthetic rates of filiform Egregia populations, however, reveal a possible devel- laterals are greater than spatulate laterals. Our studies opmental basis for variation in lateral morphology on also indicate that, per meter of axis, filiform-laden the same thallus. Filiform laterals became the domin- fronds of Egregia are 12% more productive than ant morph on longer axes, whereas spatulate morphs spatulate-covered fronds, given the higher photosyn- characterized young, short thalli and persisted on the thetic rates and greater concentrations of filiform older, basal regions of more mature and longer plants. (15.8 cm 1) versus spatulate (6.9 cm 1) laterals on This pattern of form variation in Egregia is unlike that Egregia thalli. Interestingly, this observation contradicts in other kelps where differentiation in stipe morph- results of an earlier Southern California study (Littler ology (Mann 1971, Chapman 1973), the amount of and Arnold 1982) where upper thallus segments con- blade bullation (Armstrong 1987, Roberson 2001), the sisting of filiform laterals were 32% less productive length-to-width ratios and thickness of the blades than basal portions with blade-like laterals of the same (Parke 1948, Sundene 1962a, b, 1964, Svendensen thalli. However, reduced rates for upper segments and Kain 1971, Palmisano and Sheng 1977, Gerard might have been caused by large numbers of low- and Mann 1979, Gerard 1987, Miller and Dorr 1994, producing sporophylls because Littler and Arnold’s Miller et al. 2000), or changes in the internal morph- photosynthetic experiments were performed during ology (Burrows 1964) have been associated with envi- October when, according to our studies, Southern Cal- ronmental factors, such as growing depth, wave ifornia Egregia thalli show a sharp increase in sporo- exposure, or temperature gradients. However, our ob- phyll production. servations for Southern California might not apply to Egregia menziesii is distributed across a broad latitu- Egregia populations in more northerly geographic re- dinal range in the eastern North Pacific where it shows gions where thallus and lateral morphologies can be considerable variation in its vegetative and reproduct- more variable. ive morphology (Abbott and Hollenberg 1976). Vari- Perhaps because of observations that lateral mor- ation in the vegetative lateral blades of Egregia has long phologies can vary on the same thallus, Chapman been recognized but poorly explored. Our results in- (1962a) hypothesized that filiform laterals arise from dicate a developmental basis for variation in blade EGREGIA REPRODUCTION AND MORPHOLOGY 253 morphology in Southern California populations of Methods: Macroalgae. 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In Pursuit of Bio-Criteria for Evaluating the Condition of Rocky Intertidal Communities

Report of a Workshop Sponsored by the University of Southern California Sea Grant Program with Assistance from the Bureau of Ocean Energy Management, Regulation and Enforcement

Steven N. Murray, Pete Raimondi, and Stephen B. Weisberg

Introduction

The ecological communities of California’s rocky coast are being altered by the combined impacts of coastal development, pollution, climate change, and visitor activities. Previous research has revealed that these rocky intertidal communities are dynamic and show change in response to natural (e.g., wave action, sand scour, substratum instability) and anthropogenic (e.g., effluent discharges, trampling) disturbance. Coastal managers are concerned with the status of these coastal ecological communities and are often charged with implementing procedures that protect and enhance species composition, diversity, and ecological services. They are faced with an increasing need to evaluate and monitor community change and performance, particularly with the current focus on Ecosystem-Based Management (EBM) and the implementation of the Marine Life Protection Act (MLPA). A key need is the ability to distinguish anthropogenic-driven changes in a coastal community from changes due to natural or non-anthropogenic agents. Coastal managers are seeking the metrics to determine the current condition or “health” of a site and trends in this condition over time, and to communicate this condition to the public and decision-makers in a simple manner. Ideally, this would include metrics that can be collected by citizen-scientists as well metrics or sets of metrics that can be collected by highly trained individuals. Moreover, these metrics need to be collected in a resource-limited environment. However, the development of simple metrics that reflect the condition of rocky intertidal communities has remained elusive due to the complex, dynamic, and heterogeneous nature of rocky shore ecosystems (Murray et al. 2006).

Work needs to be done to determine if parameters can be identified that represent the status of rocky shore ecosystems so monitoring and evaluation can be focused, informative, and easily communicated. Biocriteria or biotic indices have long been utilized for this purpose to evaluate the status of aquatic and terrestrial ecosystems. These criteria or indices translate environmental or biotic data into an index value or a grade, thereby breaking down complex information into an easily understandable scoring system. For example, the Index of Biological Integrity (IBI) has been employed to assess ecosystem condition in streams (Karr 1991) and soft- bottom, benthic (Weisberg et al. 1997) habitats and, similarly, the Terrestrial Index of Ecological Integrity (TIEI) has played a similar role in terrestrial ecosystems (Andreasen et al. 2001). Weisberg et al. (2008) indicate that recognized European and U.S. approaches to developing biocriteria for assessing ecological systems include: 1) comparison to historical conditions; 2) 1

comparison to present reference conditions; 3) models; and, 4) consensus (or best) professional judgment (BPJ). Rice (2003) lists the following categories of ecosystem indicators: 1) Indicator Species; 2) Diversity Indices; 3) Multivariate Ordination Techniques; and, 4) Aggregated Indicators of Ecosystem Status, and also discusses indicators that move beyond these categories and, with the aid of an ecological model, reflect emergent ecosystem properties. A key question is whether similar biocriteria or biotic indices can be developed that accurately represent the status of rocky shore ecosystems and that capture the degree to which rocky intertidal communities are disturbed by natural or anthropogenic agents.

To address this question, a team of rocky intertidal experts was convened and a three day workshop held on March 5-7 2010 at the Wrigley Institute for Environmental Science on Santa Catalina Island, California. They were joined by coastal managers and administrators of agencies and programs interested in monitoring changes in rocky intertidal populations and communities. The workshop was sponsored by the University of Southern California Sea Grant program with assistance from the Bureau of Ocean Energy Management, Regulation and Enforcement. A list of workshop participants is provided in Table 1. Table 1. Workshop Participants ------Rocky Intertidal Experts

Rich Ambrose University of California, Los Angeles Carol Blanchette University of California, Santa Barbara Jennifer Burnaford California State University, Fullerton Megan Dethier University of Washington, Friday Harbor Laboratories Jack Engle University of California, Santa Barbara Mike Foster Moss Landing Marine Lab Melissa Miner University of California, Santa Cruz Steve Murray California State University, Fullerton Karina Nielsen Sonoma State University John Pearse University of California, Santa Cruz Pete Raimondi University of California, Santa Cruz Dan Richards Channel Islands National Park Service Christy Bell University of California, Santa Cruz (Participated in Exercise but did not attend Workshop) Jayson Smith California State University, Fullerton

Managers

Dominic Gregorio State Water Resources Control Board Mary Elaine Helix Bureau of Ocean Energy Management, Regulation and Enforcement Cheri Recchia Marine Monitoring Enterprise Steve Weisberg Southern California Coastal Water Research Project Elizabeth Whiteman Marine Monitoring Enterprise

Workshop Facilitators

Phyllis Grifman University of Southern California, Sea Grant Program Susan Zaleski University of Southern California, Sea Grant Program

The specific goals of the workshop were: 1) to determine whether there would be a high level of agreement among experts in identifying disturbed (natural and anthropogenic) rocky intertidal sites using only species abundance data and meta-data describing physical site characteristics; and, 2) if so, whether these experts would make their identifications using similar approaches. An ultimate goal of the workshop was to determine which characteristics of species abundance data sets were useful for distinguishing disturbance levels for rocky intertidal sites and whether it might be possible to use these characteristics to develop criteria or an index that reflect the disturbance status of rocky intertidal populations and communities. If developed, this index will be of great benefit to managers of California’s parks, beaches, and shoreline, as well as those responsible for discharges into Areas of Special Biological Significance (ASBS), who often face difficulties in determining benchmarks for evaluating the effectiveness of their management strategies.

Prior to the workshop, a group of rocky intertidal experts was identified and asked to participate in an exercise to evaluate the condition of rocky intertidal sites using uniform data sets. This exercise was modeled after one performed for benthic infaunal communities where experts used their best professional judgment to assess the condition of 35 California soft bottom sites working only from blind data sets (Weisberg et al. 2008). In this exercise, participating experts ranked sites in a highly correlated way (r = 0.91) and achieved strong agreement on site condition. They also used similar parameters for making their assessments. In this pre- workshop exercise, each rocky intertidal expert was asked to examine common data sets containing the abundances (% cover for macro-invertebrates and macrophytes; density for mobile macro-invertebrates) of intertidal species for 31 site data sets. In addition, meta-data (substratum type, slope, relief, wave climate, sediment influence, shore expanse, and nature of nearby up and down coast habitat), and calculations of total substratum cover and measures of diversity (numbers of taxa, H’, J’, d, and 1-) were provided for each site data collection. All data sets were obtained from Pete Raimondi and his U.C. Santa Cruz intertidal sampling program.

Investigators were informed that each of the sites was located along a biogeographically uniform portion of the California coastline between Point Conception and Point Reyes. However, specific site locations were not provided and sites were identified only by number. Also unbeknown to the participants, the data included repetitive seasonal visits for five of the sampled sites. Thus, a total of 26 independent sites were investigated with data for 5 of these sites provided for two different sampling periods (Figure 1). No information describing natural disturbance (other than that deduced from the meta-data) and anthropogenic disturbance to sites was made available.

Experts were instructed to use their best professional judgment to conduct any form of analysis they found useful to examine the data and arrive at their conclusions. Each expert was to: 1) Assign each of the 31 site data sets to one of five condition categories – undisturbed, largely undisturbed, neutral, moderately disturbed, strongly disturbed – using the numerical codes for the five-point disturbance scale: undisturbed (1) to strongly disturbed (5);

2) Identify the five site data sets most strongly influenced by anthropogenic disturbance; 3) Describe the criteria (or attributes) used to arrive at the disturbance classifications together with a rating of the importance of each of these criteria; and, 4) Describe the criteria (or attributes) used to identify the five sites most strongly influenced by anthropogenic disturbance.

All expert analyses were compiled, presented to the workshop participants, and discussed to determine the degree of agreement in the site classifications and approaches used.

Figure 1. Map depicting the sites and site numbers for which data sets were supplied to experts. Note: experts were provided two temporal data sets for sites denoted by red points on the map.

Results

Identification of the Level of Site Disturbance. There was fairly good agreement among the experts in identifying the sites subjected to the greatest degree of disturbance. However, much less agreement was evident in identifying sites subjected to moderate disturbance or that received little disturbance (Table 2; Figure 2). Four site data sets (7, 8, 24 and 29) received the highest disturbance scores, averaging > 4.00 on the 5.00 scale and for Site 24 all except for one investigator scored this site as “strongly disturbed”. The data sets represented two different temporal visits to one of these four intertidal locations (sites 8 and 29). Thus, expert consensus was reached on 3 of the 26 independent sites. The site identified as the next most disturbed based on expert consensus was Site 5, followed by Sites 1, 2, and 23. Eight sites (4, 9, 12, 17, 21, 26, 28, and 30) fell on the undisturbed end of the scale based on expert scores. These sites tallied scores < 2.5. Interestingly, two of these site data sets represented sites with two seasonal visits where the experts scored one visit as less disturbed than the other. No site received more than four scores of 1 (“largely undisturbed”).

Figure 2. Average score by experts for the 31 site data sets. Sites with two separate temporal visits are 8 and 29, 2 and 27, 6 and 28, 14 and 30, and 19 and 31. Note: 5 = strongly disturbed; 4 =moderately disturbed; 3 = neutral; 2 = largely undisturbed; 1 = undisturbed.

Table 2. Results of disturbance assignments of the 13 experts (A to M). Sites are arranged from top to bottom by average score. Sites with two seasonal visits are 8 and 29, 2 and 27, 6 and 28, 14 and 30, and 19 and 31. Note: 5 = Strongly Disturbed; 4 =Moderately Disturbed; 3 = Neutral; 2 = Largely Undisturbed; 1 = Undisturbed.

Investigator

Site Number A B C D E F G H I J K L M Average 24 5 5 5 5 5 5 5 5 5 5 5 4 5 4.92 29 5 5 5 4 4 5 5 4 3 5 5 5 4 4.54 7 5 5 5 4 4 4 4 4 4 4 5 5 5 4.42 8 5 5 5 4 1 4 4 4 2 4 5 5 5 4.08 5 3 4 4 4 4 4 4 4 4 4 3 3 4 3.77 1 2 4 3 4 3 4 4 2 2 4 4 5 3 3.38 2 3 4 4 4 2 2 3 3 4 4 3 3 4 3.27 23 5 3 4 2 1 4 3 3 2 3 2 5 5 3.23 15 3 5 4 3 2 3 4 3 4 4 3 1 1 3.08 22 5 1 4 2 1 5 4 3 2 2 1 5 5 3.08 27 3 4 3 4 2 1 2 3 4 2 5 4 3 3.08 25 4 3 4 3 1 1 3 4 2 2 3 4 5 3.00 6 2 3 4 3 3 4 2 3 2 2 4 4 2 2.92 11 1 2 4 3 2 5 3 4 5 3 2 2 2 2.92 16 4 3 4 3 1 2 4 3 4 3 2 1 4 2.92 20 1 3 4 3 1 4 3 3 4 2 2 5 3 2.92 13 1 4 4 3 2 4 3 3 4 2 3 2 2 2.85 14 1 4 2 3 2 4 3 3 4 3 2 3 2 2.77 19 1 4 2 3 1 3 2 4 4 3 3 2 4 2.77 18 1 4 4 3 1 3 3 3 4 2 3 1 3 2.69 3 3 1 4 3 2 2 4 3 4 2 3 1 2 2.62 10 1 3 3 2 2 4 4 3 2 3 1 3 3 2.62 31 1 2 2 3 1 3 2 4 4 3 3 2 4 2.62 17 1 1 2 4 4 2 1 3 4 1 3 3 3 2.46 28 2 4 2 3 2 1 1 3 3 1 4 4 2 2.46 9 3 4 4 2 1 1 2 3 4 1 2 1 2 2.31 21 1 2 3 3 1 3 3 3 2 3 2 2 2 2.31 4 3 3 4 2 1 1 3 2 3 2 3 1 1 2.23 12 3 2 2 3 1 3 3 3 2 2 2 2 1 2.23 26 1 2 3 2 1 2 1 3 2 3 1 4 3 2.15 30 1 1 2 3 1 2 2 3 3 3 2 3 2 2.15 6

A problem identified in the score assignments during workshop discussions was that experts were interpreting polar ends of the disturbance scale differently, i.e., investigators differed in their interpretations of what was a Strongly Disturbed Site that merited a 5 score or an Undisturbed Site that merited a 1 score. Hence, even though investigators might similarly rank sites by levels of disturbance they might assign different numerical scores.

Identification of Sites Most Strongly Influenced by Anthropogenic Disturbance. Experts found it difficult to distinguish anthropogenic from natural or non anthropogenic-driven disturbance. Nevertheless, fairly good agreement was reached among experts in the identification of the most anthropogenically disturbed sites (Figure 3).

Figure 3. Frequency of identification of site data sets most influenced by anthropogenic disturbance by the 13 experts. Each expert Identified the 5 site data sets believed to be those most subjected to anthropogenic disturbance.

The site most frequently identified by experts to be impacted by anthropogenic disturbance was site 24. Sites 29, 8, and 7 were also often identified as being subject to anthropogenic disturbance followed by sites 22 and 23. Interestingly, all but 6 sites were named by at least one expert as being among the five most disturbed by human influence. Of the 25 listed sites, 16 sites were identified by only one of the 12 experts that submitted results for this portion of the exercise.

The most frequently identified sites (29, 24, 7, 8) were also the sites considered by the experts to be the most disturbed regardless of whether disturbance stemmed from natural or anthropogenic sources. In fact, there was a strong correlation (r = 0.88) between the average score for a site on the five point disturbance scale and the frequency with which a site was identified as being disturbed by anthropogenic agents (Figure 4).

Figure 4. Correlation between the average scores for a site based on the five-point disturbance scale and the frequency with which a site was identified by experts as being among the five sites most subjected to anthropogenic disturbance. Five of the 26 independent sites were not identified as being among the top five subjected to anthropogenic disturbance.

Approaches Used by Experts to Place Sites on a Disturbance Scale. Working solely from the provided data, experts used a variety of approaches and criteria to identify the degree of disturbance, regardless of source, affecting each of the 31 site data sets. No guidance was given so each expert’s approach and decision-making was independent. Nevertheless, there was a high degree of similarity in the key criteria identified by experts in making their evaluations of site disturbance. The approaches and criteria used can be condensed into five categories (Table 3). These were consistent with the criteria and approaches used previously (see Rice 2003) to assess ecosystem condition and included: 1) ordination methods drawing on the full use of all biotic data, e.g., community-level analyses using multivariate statistics; 2) the relative cover of biota and bare rocky substratum; 3) the abundance profiles of specific species populations and types of species; 4) community diversity; and 5) the prevalence of selected physical factors. Most experts used multiple criteria in developing their site disturbance scores.

Table 3. Summary of approaches and criteria used by experts to identify the degree of disturbance, regardless of source, affecting site data sets. Approach or Criteria Examples Community-Level Analyses Cluster Analysis and MDS mostly using cover data Overall Cover Patterns Disturbance Indicators: Low Biotic Cover; High Bare Rock Cover Diversity Disturbance Indicator: Low Diversity (Numbers of Taxa, H’, 1- , Family Richness) Abundances of Species Disturbance Indicators: High Cover of Opportunistic Seaweeds Groups or Selected Taxa (e.g., Ulva, Filamentous, Sheet, and Tubular Algae); Low Cover of Rockweeds; High Abundances of Mussels, Sea Stars, Limpets; Low Abundances of Black Abalone, Sea Grasses, and Corticated Algae; Absence of Certain Species; Deviations from Expected Abundance Patterns Physical Factors Disturbance Indicator: High Sand Cover or Scour; High Wave Exposure; Unstable Substratum (e.g., Cobble)

Approaches Used by Experts to Identify the Sites Most Subject to Anthropogenic Disturbance. Experts uniformly expressed concern about identifying the 5 sites most subject to anthropogenic disturbance among the 31 site data collections examined and in identifying the criteria used. Of principal concern was the ability to distinguish between natural and anthropogenic disturbance and the acknowledgement that multiple disturbance agents affect rocky intertidal sites so distinguishing natural from anthropogenic drivers becomes problematic. Two other issues arose during discussions of the identification of anthropogenically-disturbed sites. The first was that there appeared to be a narrow range of anthropogenic disturbance affecting the sites examined in the exercise. This could be addressed by including sites that represented a wider range of site types with respect to anthropogenic disturbance in a subsequent exercise. The second was that biological parameters are affected differently by different types of anthropogenic disturbance. Hence, it is difficult to key in on data indicators without knowing the type of anthropogenic disturbance. Experts agreed that addressing this topic requires more study and work.

Exercise Challenges. There were two primary exercise challenges identified during the workshop discussions: 1) Experts used variable definitions of “disturbance”. Some considered “natural” disturbance part of the natural state of a system, so a site with high levels of wave action, for example, was considered by some to be not very disturbed because this is part of its natural state. Whereas, participants, using this same information, categorized this type of site as highly disturbed. The definition of “natural” disturbance and how one categorizes this disturbance is essential for creating an index that represents site condition and reflects anthropogenic driven changes from the expected natural state.

2) Experts variously interpreted the thresholds separating the five assessment categories when scoring the degree of disturbance. The scale for ranking sites from 1 to 5 was 9

not clearly defined, so this left room for individual expert interpretation. For example, some experts failed to rank any site as “largely undisturbed”, whereas others assigned “strongly disturbed” rankings to only one site in the exercise. As a consequence, while good agreement was reached on the most disturbed sites, much less agreement was achieved in the disturbance scores for less disturbed sites and the inter-investigator correlation (r = 0.34) established from expert scores was relatively low. Participants agreed that with clearer more uniform interpretations of the five point disturbance scale, much better agreement would likely be realized.

Deviations from Expected Site Conditions. Rocky intertidal habitats vary greatly from site to site based on biogeography and physical site features, including exposure to non-anthropogenic forms of natural disturbance. Experts agreed that these factors must be addressed in order to develop an index that describes the status of a site with respect to anthropogenic impact. In this exercise, sites were located within a uniform biogeographic region to eliminate geographic changes in biota such as between central and southern California. Physical variations in site features (e.g., wave exposure, sand influence, and substratum type, slope, and relief) were present and needed to be accounted for by experts in making their assessments. Thus, the challenge for making a determination of site condition and the degree to which a site was exposed to anthropogenic disturbance was to evaluate the suite of biological characteristics (e.g. species abundances, diversity, etc.) against what was believe to be the expected condition. Then, deviations from this expected condition could be used to assess site status. This approach would enable managers to identify sites that have drifted from expected conditions but would not determine causality. This approach requires understanding of:

1) Normal variation expected within each site type 2) The ends of the spectrum along the site condition scale 3) Past or current conditions used to set the end of the spectrum where the site was free from anthropogenic influences.

Future Work. Given the progress made at this workshop, the participants agreed that a follow-up exercise and ensuing workshop would be productive. Participants concluded that the ratings of a site data set were more based on differences in how an expert defined and categorized disturbance and determined the disturbance level on the five-point scale compared with the actual data-based characterization of the site. A principal purpose of a follow-up exercise would be to overcome interpretational differences among experts in rating sites and to make further progress in identifying the metrics that could best be used to describe site condition. This will require discussion of the expected biological characteristics of sites under different types and degrees of environmental “disturbance”. The follow-up exercise should be similarly constructed, including data from a range of sites unknown to the experts and should include additional, strongly disturbed site data sets to provide a wider range of conditions to evaluate. In addition, the disturbance scale should be more clearly defined to reduce the variation in a score given to a site data set viewed similarly by experts in terms of disturbance level. In this follow-

up exercise, experts should also be asked to rank sites from first to last on the more clearly defined disturbance scale.

Summary of Consensus Outcomes. The results of the workshop were promising and several consensus outcomes were realized. In summary these were: 1) Rocky intertidal habitats vary greatly from site to site based on non-anthropogenic environmental drivers making simple assessments of the status of these sites complex; 2) There are some common characteristics and approaches that experts used to come up with their assessments of each site; 3) Definitions are needed to clearly articulate what is meant by “disturbance”, including anthropogenic driven “disturbance”; 4) The scale for scoring disturbance, including its end points, needs to be clarified to eliminate noise resulting from investigator interpretation; 5) Once “natural” environmental characteristics are accounted for, sites would be expected to display a suite of biological characteristics (e.g. species abundances, diversity, etc.) that would represent the expected condition and then deviations from this expected condition could be used to describe site status; 6) Establishing an index to capture the condition of rocky intertidal sites appears feasible and is worth pursuing.

Literature Cited

Andreasen, J. K., O’Neill, R. V. O., Noss, R., and Slosser, N. C. 2001. Considerations for the development of a terrestrial index of ecological integrity. Ecological Indicators 1: 21-35.

Murray, S. N., Ambrose, R. F., and Dethier, M. N. 2006. Monitoring rocky shores. University of California Press, Berkeley, California.

Karr, J. R. 1991. Biological integrity: a long-neglected aspect of water resource management. Ecological Applications 1: 66-84.

Rice, J. 2003. Environmental health indicators. Ocean & Coastal Management 46: 235-259.

Weisberg, S. B., Ranasinghe, J. A., Dauer, D. M., Schaffner, L. C., Diaz, R. J., and Frithsen, J. B. 1997. An estuarine benthic index of biotic integrity (B-IBI) for Chesapeake Bay. Estuaries 20: 149-158.

Weisberg, S. B., Thompson, B., Ranasinghe, J. A., Montagne D. E., Cadien, D. B, Dauer, D. M., Diener, D., Oliver, J., Reish, D. J., Velarde, R. G., and Word, J. Q.. 2008. The level of agreement among experts applying best professional judgment to assess the condition of benthic infaunal communities. Ecological Indicators 8: 389-394.

Consistent Frequency of Color Morphs in the Sea Star Pisaster ochraceus (Echinodermata:Asteriidae) across Open-Coast Habitats in the Northeastern Paciﬁc1

Peter T. Raimondi,2 Raphael D. Sagarin,3,4 Richard F. Ambrose,5 Christy Bell,2 Maya George,2 Steven F. Lee,5 David Lohse,2 C. Melissa Miner,2 and Steven N. Murray6

Abstract: The sea star Pisaster ochraceus (Brandt, 1835) is among the most conspicuous members of northeastern Pacific rocky-shore fauna due to its dramatic color variation, ranging from bright yellowish orange to brown to deep purple. Despite a large body of ecological and developmental biology information on P. ochraceus, few studies have rigorously examined color patterns or their causes across its geographic range. We used thousands of observations of sea star color and size taken from southern California to northern Oregon to show that the frequency of orange sea stars is approximately 20% with little variation across a broad latitudinal band. However, the frequency of orange sea stars in a population increases with the size of the animals in most populations. We consider several alternative hypotheses for these color patterns but find that the most par- simonious explanation is that adult color is a selectively neutral genetic trait that expresses itself ontogenetically. These novel findings point to the need for re- newed study of the basic biology of this key ecological species.

One of the most immediately conspicuous perienced intertidal biologists have observed observations in northeastern Pacific tide pools that about one-fourth to one-third of the is the striking color differences in the sea star P. ochraceus in any given site along the open Pisaster ochraceus (Brandt, 1835). Even at a Pacific coast are orange, and the remainder distance one can easily pick out orange and are some variant of brown, rust, or purple purple sea stars as they line the rock walls (E. Sanford, J. Pearse, R. Strathmann, and near intertidal mussel beds. Anecdotally, ex- C. Harley, pers. comm. to R.D.S. 2004). Although P. ochraceus is one of the most extensively studied intertidal invertebrates, with many published studies, for example, on 1 This is contribution number 226 of the Partnership its development (George 1999), physiology for Interdisciplinary Studies of Coastal Oceans (PISCO) funded primarily by the Gordon and Betty Moore Foun- (Vasu and Giese 1966), diet (Feder 1959, dation and the David and Lucile Packard Foundation. Menge 1972), effects on prey species Manuscript accepted 9 June 2006. (Mauzey et al. 1968), parasitism (Leighton 2 Long Marine Laboratory, University of California, et al. 1991), settlement patterns (Sewell 100 Shaffer Road, Santa Cruz, California 95060. 3 Corresponding author (e-mail: rafe.sagarin@duke and Watson 1993), role as a ‘‘keystone’’ .edu). species (Paine 1966, Menge et al. 2004) and 4 Nicholas Institute for Environmental Policy Solu- in maintaining alternate community states tions, Duke University, Durham, North Carolina 27708. (Paine and Trimble 2004), and reactions 5 University of California, Department of Environ- to climatic change (Sanford 1999), remark- mental Health Sciences, Los Angeles, California 90095- 1772. ably little is known about the basic bio- 6 Department of Biological Science and College of logical foundations of its color variants nor Natural Sciences and Mathematics, California State Uni- the ecological conditions that support pheno- versity, Fullerton, Fullerton, California 92834-6850. typic color polymorphism in this sea star. Most of what we know about color morphs Pacific Science (2007), vol. 61, no. 2:201–210 in P. ochraceus stems from studies done more : 2007 by University of Hawai‘i Press than half a century ago on small numbers of All rights reserved individuals from just one or two locations.

201 202 PACIFIC SCIENCE . April 2007

Fox and Scheer (1941) confirmed that color (Nevo 1973, Hairston 1979, Etter 1988); and in P. ochraceus is determined by two carot- (4) balancing trade-offs among these agents. enoid pigments, suggesting that diet plays a Mechanisms invoking plasticity include the role in coloration because animals generally roles of (1) color plasticity in response to do not produce carotenoids. Beyond that pa- environmental factors (Wente and Phillips per, an unpublished study of variation in 2003); (2) dietary differences resulting in color polymorphism by Forbes (1951), and a phenotypic differences (Tlusty and Hyland review by Fox and Hopkins (1966), none of 2005); and (3) ontogenetic color change the 128 published works on P. ochraceus in- (Booth 1990). dexed by ISI Web of Knowledge between With so many potential mechanisms, it 1910 and 2005 nor the citations on P. ochra- may not be logistically feasible to study color ceus reviewed in Intertidal Invertebrates of Cal- polymorphism in a species across a large ifornia (Morris et al. 1980) addressed color range using detailed mechanistic experiments patterns in P. ochraceus or the mechanisms such as those used on smaller scales or on eas- for them. ily manipulated study systems (e.g., labora- Phenotypic color polymorphism in other tory experiments with guppies). However, a organisms has been commonly observed (En- common theme to almost all alternative hy- dler 1986, Galeotti et al. 2003, Wente and potheses is that color morphs are segregated Phillips 2003) and has generated numerous into different spatial, temporal, ontogenetic evolutionary explanations for why sometimes or behavioral niches for which the different strikingly different colors should be main- color morphs are better adapted. This sug- tained. In almost all studies, the null hypoth- gests that broad-scale observations of color esis that color polymorphism is selectively morphs taken across an environmental gradi- neutral has been rejected. Although color ent containing many of these niches, com- polymorphism without an obvious selective bined with an understanding of the natural mechanism is unexpected, it is not unprece- history of an organism, can begin to elim- dented. Oda and Ishii (2001) demonstrated inate the likelihood of certain hypotheses that color polymorphism in Conocephalus mac- while suggesting more-likely hypotheses that ulatus katydids is genetically determined but could be addressed with specific mechanistic not under environmental selection, and Finke studies. Here we use an unprecedented num- (1994) found no sexual, apostatic, or disrup- ber of color and size observations obtained tive selective mechanisms acting on female over a wide latitudinal gradient to examine al- color dimorphism in Enallagma damselflies. ternative hypotheses related to the mainte- Alternative hypotheses generally can be nance of color polymorphism in P. ochraceus. classified as invoking either selective mechanisms that have a persistent effect on popula- materials and methods tions or transient mechanisms that rely on a phenotypically plastic trait. Alternative hy- Samples of Pisaster ochraceus size and color potheses with empirical support based on se- were taken by three different groups of inves- lective mechanisms include (1) nonrandom tigators that share data as part of the Multi- mating due to sexual selection or signaling Agency Rocky Intertidal Network (MARINe) to prevent inbreeding (Houde 1987, Galeotti and the Partnership for Interdisciplinary et al. 2003); (2) apostatic selection, in which Studies of Coastal Oceans (PISCO). Samples rare morphs are more successful in hunting were taken biannually between fall 2000 and prey or avoiding predators through the dis- fall 2003 at 26 sites located between southern ruption of search images or advertisement California (33.71 N) and northern Oregon of distastefulness (Allen 1988, Gillespie and (45.92 N) within permanent demarcated Oxford 1998, Horth 2004); (3) disruptive plots in the low intertidal (Figure 1). Sizes of selection through crypsis in heterogeneous the plots varied with site, ranging from 20 backgrounds or physiological adaptation to to 160 m2, depending on geomorphology spatially or temporally variable environments and available habitat. Because our goal was Figure 1. Map of 26 study sites along the west coast of North America. 204 PACIFIC SCIENCE . April 2007 specifically to measure and record the color 0.879, P <:001) and width of the largest of many individuals at each site, plots were arm (Pearson correlation coefficient ¼ 0.904, chosen to represent a range of habitat types P <:001), indicating that maximum radius is (e.g., low intertidal crevices, rock walls, and representative of size. pools) where P. ochraceus of all postsettlement Our analysis was designed to focus on life stages can be found, rather than a strati- color ratios and to avoid issues of noninde- fied random plot design (which would be pendence that might arise from repeatedly more appropriate if the goal was to compare sampling individuals in permanent quadrats. population size estimates). Hence, at each site we calculated the percent- Sites were sampled by MARINe re- age of orange individuals for each sample pe- searchers from University of California, Los riod and then averaged those percentages to Angeles (UCLA), and the University of Cali- produce an overall site average. To examine fornia, Santa Cruz (UCSC), and PISCO re- the percentage of orange individuals in popu- searchers from UCSC. Because our sampling lations of different sizes the mean number of methodology is relatively simple and was con- purple and orange individuals for each 10- ducted by experienced intertidal researchers mm size bin across all sample periods was who frequently communicate about sampling calculated for each site. Means were then issues, differences due to observer bias in re- summed for these color categories across all cording color or size across sites is unlikely. sites and the percentage of orange morphs Our study sites are wave-exposed open was calculated. By aggregating our data, the coast areas that represent the most common potential problem of near-zero or zero values P. ochraceus habitat over most of its geo- in the smallest and largest size categories was graphic range. We also used additional ob- avoided. servations by ourselves and others from Finally, habitat use, aggregation by color, protected-water sites in Puget Sound (Wash- and seasonal differences in color ratios were ington State) and Vancouver Island, British tested using quantitative analyses (chi square Columbia, to gain insight into the open-coast and analysis of variance [ANOVA]), special- patterns we report. Along the 1,850-km ized data collection efforts, and through qual- stretch of open coast from Baja California to itative observations made during sampling Oregon, and farther north, sea stars generally visits. occur in orange, purple, and brown color morphs. All sampled sea stars were measured results and discussion and scored for color as either ‘‘orange’’ or ‘‘purple’’ (all brown and darker shades were The monitoring data analyzed here, incorpo- scored in the ‘‘purple’’ category because field rating 14,720 observations of Pisaster ochra- tests determined that brown and purple forms ceus, demonstrate both consistency of orange are difficult to differentiate consistently). Al- color frequencies in adult sea stars over a though there is considerable color variation broad latitudinal gradient (Figure 2) and among the darker forms in this species, we changes in the frequency of orange morphs use this simple orange/purple dichotomy in from small to large sea stars at most sites our observations and analysis because it is (Figure 3). The range in percentage orange least likely to introduce sampling bias while morphs for all sites was 12.6–27% (mean ¼ still offering the ability to evaluate the orange 20:0 G 4:4% SD). Regression of percentage color morph patterns observed in the field. orange against size was positive and highly Size measurements were made with cali- significant (R2 ¼ 0:74, P <:001). pers or rulers from the tip of the longest arm Observations of 177 individuals from to the center of the aboral disk and recorded Hopkins Marine Station (central California) to the nearest 10 mm. Pilot data from 438 in- and Old Stairs (southern California) showed dividuals confirmed a strong correlation be- no relationship between color and habitat tween this radial measurement and oral disk type (flat benches, vertical walls, or shaded radius (Pearson correlation coefficient ¼ crevices) (Pearson chi-square ¼ 1.38, df ¼ 2, Patterns of Color Morphology for Pisaster ochraceus . Raimondi et al. 205

Figure 2. Average percentage of orange sea stars (GSE) in the population at all sites, arranged from south to north.

P ¼ :501). Similarly, clustering of color results are in accordance with qualitative ob- morphs was not detected because 24% of servations of the frequency of color morphs nonorange sea stars were found closest to or- in this species that we made during hundreds ange individuals and 78% of orange sea stars, of sampling visits. Finally, we found no evi- mirroring the overall color frequencies, were dence of consistent seasonal differences in found closest to nonorange sea stars. These the percentage of P. ochraceus orange color morphs in our sampled populations (AN- OVA, F ¼ 1:09, df ¼ 45, P ¼ :364).

Selective Mechanisms The wealth of knowledge on P. ochraceus raises doubts about hypotheses that invoke selective mechanisms as viable explanations for color polymorphism in this species. These sea stars are dioecious, broadcast spawners with little visual ability beyond sensing light and dark (Morris et al. 1980). Hence, it is unlikely that color serves as a cue for sexual or other forms of visually based selection. The sea star’s main prey items are sessile and use only size as an escape from predation, Figure 3. Percentage of orange sea stars in increasing or use their mobility to escape by responding size bins. The mean number of purple and orange indi- to chemical traces of the predator in the viduals for each 10-mm size bin across all sample periods was calculated at each site. Means were summed for each water (Phillips 1975, Morris et al. 1980). color across all sites and percentage orange was calcu- Thus, color differences would not afford any lated. color morph an advantage in obtaining prey. 206 PACIFIC SCIENCE . April 2007

Among larger (>30-mm radius) individuals, discontinuities in larval supply. These ﬁnd- no P. ochraceus color morph is cryptic in inter- ings suggest that genetic drift is not likely to tidal habitats. Greater mortality in purple P. play a dominant role in affecting color morph ochraceus could lead to an increase in the fre- frequencies. quency of orange sea stars in a population. Nonetheless, a limited temporal and spa- However, predation on sea stars is not com- tial perspective could mask selective pressures monly observed, although sea otters prey on affecting these populations. For example, sub- P. ochraceus, and seagulls are occasionally tidal populations, which were not sampled, observed pulling sea stars off intertidal rocks. could have different overall color ratios due If relying on visual cues (whether color or to selective pressures on color. However, this monochromatic), these visual predators would appears even less likely than in intertidal likely target the more conspicuous orange sea habitats because P. ochraceus would be less af- stars, which contrast more strongly with the fected by environmental conditions such as coloration patterns of intertidal habitats. Al- heat stress while immersed and coloration though it is plausible that experience with sea could only be affected by selective sea otter stars or some color-speciﬁc olfactory signal predation at the small number of our sites could impart a preference for purple stars if supporting otter populations. Alternately, orange stars are less palatable, to date no one color polymorphisms observed at one time has investigated this hypothesis. However, as may be under selection toward the domi- Ricketts and Calvin (1939:116–117) explained, nance of one form (e.g., Stolz et al. 2003). ‘‘Pisaster neither has nor seems to need pro- The samples we analyzed do not represent a tective coloration. Anything that can damage time series long enough to determine conclu- this thoroughly tough animal, short of the sively if the observed color ratios vary over ‘acts of God’ referred to in insurance policies, time. However, observations of color ratios deserves respectful mention.’’ of 1,327 P. ochraceus (across all sizes) by biol- Across the geographic range of our ogy student Clifford Forbes in 1951 indicated study sites, intertidal communities experience orange frequencies of 20% in Trinidad, Cali- widely different climatic conditions, tidal re- fornia (41.07 N), and 25% at Hopkins gimes, and species assemblages, and yet the Marine Station (36.62 N) (Forbes 1951), ratio of orange morphs to other color vari- mirroring the values we observed in our ants remains similar. Moreover, the different samples. color morphs of P. ochraceus do not segregate into different niches—spatially, temporally, Size-Related Plasticity or behaviorally. Our observations collected over 120 sampling visits, as well as those of The size-related shift in the frequency of or- numerous intertidal ecologists, suggest that ange color morphs, which has not previously color morphs do not separate into different been documented, seems to indicate pheno- intertidal habitats, nor do they aggregate typic plasticity in this trait. The color shift preferentially, or show a seasonal component could arise from diet, ontogenetic differences to color dominance. These observations were in mortality, or ontogenetic color change. supported by our more-detailed scoring of Adults of both color morphs were consis- habitat use and aggregation by color at Hop- tently observed congregating on the same kins Marine Station and Old Stairs sites, as prey items (e.g., Mytilus californianus). Feder well as the quantitative analysis of our data (1959) demonstrated that regardless of geo- parsed by season. Finally, populations appear graphic location or habitat, P. ochraceus over- to be well mixed genetically across their whelmingly eats the prey it is primarily found range. Recent work by Harley et al. (in press) with, suggesting that these sea stars feed pri- revealed no geographic genetic population marily on the California mussel (M. califor- structure across the species range, even when nianus) throughout its range. Nonetheless, P. comparing locations on alternate sides of ochraceus also will feed opportunistically on known biogeographic boundaries or known many other prey items in our study range Patterns of Color Morphology for Pisaster ochraceus . Raimondi et al. 207

Figure 4. Purple (left) and orange (right) Pisaster ochraceus photographed at low tide at Carpinteria, California, March 2004, by R.D.S. Scale bar approximately 10 cm. Note purple (dark) arm tips on the orange sea star.

(E. Sanford, pers. comm. 2006). Although curs in other taxa (Booth 1990). Although di- it is conceivable that mussels of different rect observations of color change have not quality (e.g., reproductive individuals) might been made, support for ontogenetic color affect color or that alternative prey items change in P. ochraceus comes from frequent might impart different color pigments to observations of intermediate-size orange sea their predators, it is not clear how (or why) stars with purple arm tips (Figure 4), and only one sea star color morph would con- observations of orange stars regenerating a sistently target one type of mussel or alterna- mostly purple arm bud. Ontogenetic color tive food source. However, food sources of change in limited parts of an organism’s body juvenile P. ochraceus, which are unknown, has been observed in other marine inverte- might ultimately affect adult color patterns. brates (e.g., Tlusty and Hyland 2005). The In lobsters, for example, juvenile diet has delayed onset of orange coloration may be been shown to affect color patterns through related to the cryptic coloration afforded to both genetically determined and phenotypi- very small (<30 mm), nonorange-colored sea cally plastic pathways (Tlusty and Hyland stars on coralline algae in our study range, 2005). where they are often found as newly settled Hypothetically, P. ochraceus could change recruits. This is analogous to Cancer irroratus color ontogenetically, a phenomenon that oc- rock crabs, where coloration is conspicuous in 208 PACIFIC SCIENCE . April 2007 adults but cryptic in newly settled juveniles Wave exposure, water chemistry, and (Palma and Steneck 2001). Moreover, other available food resources differ substantially investigators (E. Sanford, pers. comm. 2006) between protected and outer-coast sites. Lo- and we ourselves have noted that most small cal differences in wave exposure might be- (e.g., <30 mm) sea stars tend to be grayish come manifest through differences in larval purple or grayish brown along the exposed settlement patterns. In the embayments of Pacific coast, indicating that adult purple and Puget Sound and other protected waters, brown stars also change color but perhaps not founder effects might dominate so that infre- as dramatically as orange adults. Apparently, a quent settlement events skewed by chance to- different pattern is seen in some habitats in ward one color morph or another could result the northeastern Pacific where small sea stars in similarly skewed adult sea star populations. are more commonly orange, a color that is This hypothesis is supported by data on the more cryptic on their preferred settlement size structures of P. ochraceus populations at habitat there (R. Paine, pers. comm.), but six San Juan Island sites, which showed that extensive observations of color ratios at dif- sea stars <70-mm radius were absent from ferent sizes have not been made for those 250 sampled individuals compared with 27% populations. of all observations for the open coast. This finding suggests that recruitment events are more episodic in these protected waters. Sa- Differences with Protected-Water Populations linity and pH are likely to be different in protected waters compared with open-coast sites, The frequencies of color morphs in P. ochra- but at present we do not know the effects ceus populations from protected waters in the of water chemistry on sea star pigmentation. northeastern Pacific are in stark contrast to Pisaster ochraceus populations in quiet water those we observed for open-coast popula- environments also likely differ from open- tions, which might shed light into the mecha- coast populations in diet, because Mytilus cal- nisms underlying color polymorphism in this ifornianus, a prominent bed-forming space oc- species. First, protected-water populations are cupier on much of the open Pacific coast, is much more variable in color ratios, and indi- not found in great densities on San Juan Is- vidual sites tend to be dominated by one color land or at other protected-water sites. Differ- morph or another. For example, on San Juan ences in diet could hypothetically result in Island (48.5 N, 123 W ), purple stars domi- different color ratios and different color tones nate. Of 250 individuals sampled at six sites in open- versus protected-water populations, on San Juan Island by R.D.S. in September but dietary differences do not explain how 2005, only 4.8% were orange. Likewise, polymorphism is maintained with such con- purple individuals dominate populations in sistency across the broad geographic range Georgia Strait (D. Eernisse, pers. obs.) (Har- represented by our outer-coast study sites. ley et al. in press) and at sites along the Inside Moreover, observations from protected-water Passage of southeastern Alaska (C. Baxter, populations must be taken with caution be- pers. obs.). Yet, on Orcas Island, adjacent to cause it has been suggested (Ricketts et al. San Juan Island, populations are dominated 1985) that these populations are a subspecies by orange individuals (R. Strathmann, pers. of P. ochraceus (i.e., P. ochraceus confertus). obs.). In addition, the purple stars in these protected-water populations are far more conclusions and future directions vivid than their open-coast counterparts, although small numbers of brightly colored In 1959, Feder lamented, ‘‘Although the star- purple stars have been observed at open-coast fish Pisaster ochraceus is one of the most con- sites (E. Sanford, pers. comm.). At protected spicuous animals to be found along the rocky sites, orange individuals are much paler in shores of the Pacific Coast . . . its natural color, and the brown color morph seen on the history is poorly known’’ (Feder 1959:721). open coast is largely absent (RDS, pers. obs.). Nearly 50 yr later, because of Feder and Patterns of Color Morphology for Pisaster ochraceus . Raimondi et al. 209 others, knowledge of the natural history Literature Cited of P. ochraceus has increased, but causes of a most obvious characteristic—its striking color Allen, J. A. 1988. Frequency dependent selec- polymorphism—remains a mystery. tion by predators. Philos. Trans. R. Soc. Several of the key questions raised by our Lond. B Biol. Sci. 319:485–503. observations can become the focus of a re- Booth, C. L. 1990. Evolutionary significance newed effort to understand patterns of color of ontogenic color change in animals. Biol. in P. ochraceus. Elucidation of the gene(s) and J. Linn. Soc. 40:125–163. pigment complexes responsible for color is a Endler, J. 1986. Natural selection in the fundamental gap in our understanding of wild. Princeton University Press, Prince- color patterns. Mating experiments involving ton, New Jersey. crosses of variously colored parents might Etter, R. J. 1988. Physiological stress help determine the inheritance patterns of and color polymorphism in the intertidal color, although typically high mortality in snail Nucella lapillus. Evolution 42:660– laboratory cultures may confound interpreta- 680. tion of results. Basic biological questions need Feder, H. M. 1959. The food of the starfish, to be assessed in an ecological context, con- Pisaster ochraceus, along the California sidering how variation in diet, water chemis- coast. Ecology 40:721–724. try, and biological interactions can affect Finke, O. M. 1994. Female colour polymor- pigmentation and the occurrence and mecha- phism in damselflies: Failure to reject the nisms of color change. Moreover, under- null hypothesis. Anim. Behav. 47:1249– standing the extent to which larval dispersal 1266. effectively mixes populations will provide in- Forbes, C. 1951. A survey of Pisaster ochraceus sight into the role that genetic drift could colors in separated regions. University play in skewing color ratios. Clarification of of California, Berkeley. Available from population genetic structure and phylogeo- Hopkins Marine Station Library, Pacific graphic patterns will help to address the ques- Grove, California 93950. tion of whether protected-water populations Fox, D. L., and T. S. Hopkins. 1966. The are genetically distinct from one another and comparative biochemistry of pigments. from open-water populations. Although ad- Pages 277–300 in R. A. Boolootian, dressing these questions will be a challenge, ed. Physiology of Echinodermata. Inter- improved understanding of the mechanisms science, New York. of color variation in this common sea star Fox, D. L., and B. T. Scheer. 1941. Com- would be greatly appreciated by the many parative studies of the pigments of some amateur naturalists and professional biologists Pacific coast echinoderms. Biol. Bull. who have been intrigued by this conspicuous (Woods Hole) 80:441–455. tide-pool animal. Galeotti, P., D. Rubolini, P. O. Dunn, and M. Fasola. 2003. Colour polymorphism in acknowledgments birds: Causes and functions. J. Evol. Biol. 16:635–646. We thank D. Eernisse, C. Harley, B. Menge, George, S. B. 1999. Egg quality, larval J. Pearse, E. Sanford, and R. Strathmann for growth and phenotypic plasticity in a for- sharing their knowledge of Pisaster ochraceus. cipulate seastar. J. Exp. Mar. Biol. Ecol. J. Wible of the Miller Library at Hopkins 237:203–224. Marine Station provided research assistance. Gillespie, R. G., and G. S. Oxford. 1998. Se- Research in San Juan Island was conducted lection of the color polymorphism in Ha- with the Beam Reach Science and Sustain- waiian happy-face spiders: Evidence from ability Field School. Research by the Multi- genetic structure and temporal fluctua- Agency Rocky Intertidal Network (MARINe) tions. Evolution 52:775. was sponsored by the U.S. Minerals Manage- Hairston, N. G. 1979. 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cies of Diamptomus (Copepoda). Limnol. Paine, R. T., and A. C. Trimble. 2004. Oceanogr. 24:15–37. Abrupt community change on a rocky Harley, C. D. G., M. S. Pankey, J. P. Wares, shore—biological mechanisms contribu- M. J. Wonham, and R. K. Grosberg. In ting to the potential formation of an alter- press. Color polymorphism and genetic native state. Ecol. Lett. 7:441–445. structure in the sea star Pisaster ochraceus. Palma, A. T., and R. S. Steneck. 2001. Does Biol. Bull. (Woods Hole). variable coloration in juvenile marine crabs Horth, L. 2004. Predation and the persis- reduce risk of visual predation? Ecology tence of melanic male mosquitofish (Gam- 82:2961–2967. busia holbrooki). J. Evol. Biol. 17:672–679. Phillips, D. W. 1975. Distance chemorecep- Houde, A. E. 1987. Mate choice based upon tion-triggered avoidance behavior of lim- naturally occurring colour-pattern vari- pets (Acmaea). J. Exp. Zool. 191:199–209. ation in a guppy population. Evolution Ricketts, E. F., and J. Calvin. 1939. Between 41:1–10. Pacific tides. Stanford University Press, Leighton, B. J., J. D. G. Boom, C. Bouland, Stanford, California. E. B. Hartwick, and M. J. Smith. 1991. Ricketts, E. F., J. Calvin, and J. W. Hedg- Castration and mortality in Pisaster ochra- peth. 1985. Between Pacific tides. Stanford ceus parasitized by Orchitophrya stellarum University Press, Stanford, California. (Ciliophora). Dis. Aquat. Org. 10:71–73. Sanford, E. 1999. Regulation of keystone Mauzey, K. P., C. Birkeland, and P. K. Day- predation by small changes in ocean tem- ton. 1968. Feeding behavior of asteroids perature. Science (Washington, D.C.) and escape responses of their prey in the 283:2095–2097. Puget Sound region. Ecology 49:603–619. Sewell, M. A., and J. C. Watson. 1993. A Menge, B. A. 1972. Competition for food be- ‘‘source’’ for asteroid larvae?: Recruitment tween two intertidal starfish species and its of Pisaster ochraceus, Pycnopodia helianthoides effect on body size and feeding. Ecology and Dermasterias imbricata. Mar. Biol. 53:635–644. (Berl.) 117:387–398. Menge, B. A., C. Blanchette, P. Raimondi, T. Stolz, U., S. Velez, K. Wood, M. Wood, and Freidenburg, S. Gaines, J. Lubchenco, D. J. Feder. 2003. Darwinian natural selection Lohse, G. Hudson, M. Foley, and J. Pam- for orange bioluminescent color in a Ja- plin. 2004. Species interaction strength: maican click beetle. Proc. Natl. Acad. Sci. Testing model predictions along an up- U.S.A. 100:14955–14959. welling gradient. Ecol. Monogr. 74:663– Tlusty, M., and C. Hyland. 2005. Astaxanthin 684. deposition in the cuticle of juvenile Amer- Morris, R. H., D. P. Abbott, and E. C. Ha- ican lobster (Homarus americanus): Impli- derlie. 1980. Intertidal invertebrates of cations for phenotypic and genotypic California. Stanford University Press, Stan- coloration. Mar. Biol. (Berl.) 147:113–119. ford, California. Vasu, B. S., and A. C. Giese. 1966. Protein Nevo, E. 1973. Adaptive color polymorphism and non-protein nitrogen in the body fluid in cricket frogs. Evolution 27:353–367. of Pisaster ochraceus (Echinodermata) in Oda, K.-I., and M. Ishii. 2001. Body color relation to nutrition and reproduction. polymorphism in nymphs and adults of a Comp. Biochem. Physiol. 19:351–361. katydid, Conocephalus maculatus (Orthop- Wente, W. H., and J. B. Phillips. 2003. tera: Tettigoniidae). Appl. Entomol. Zool. Fixed green and brown color morphs and 36:345–348. novel color-changing morph of the Pacific Paine, R. T. 1966. Food web complexity and tree frog Hyla regilla. Am. Nat. 162:461– species diversity. Am. Nat. 100:65–75. 473. Journal of Sea Research 61 (2009) 165–173

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Journal of Sea Research

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Spatial patterns in recruitment and growth of the mussel Mytilus californianus (Conrad) in southern and northern California, USA, two regions with differing oceanographic conditions

Jayson R. Smith a,⁎, Peggy Fong a, Richard F. Ambrose b a Department of Ecology and Evolutionary Biology, University of California Los Angeles, 621 Charles E. Young Dr., South, Los Angeles, CA 90095-1606, United States b Environmental Science and Engineering Program, Department of Environmental Health Sciences, University of California Los Angeles, Box 951772, Los Angeles, CA 90095-1772, United States article info abstract

Article history: Mussels, Mytilus californianus, and other benthic invertebrate populations on the wave-exposed intertidal Received 1 August 2007 coast of the eastern North Paciﬁc are impacted by a suite of biotic and abiotic factors on both local and larger Received in revised form 6 October 2008 geographic scales. Previous surveys of mussel abundances along the California coast have revealed that Accepted 16 October 2008 mussels, in general, are very abundant in northern California while low in southern California. Nevertheless, Available online 25 October 2008 mussel abundances in southern California are highly variability with a small number of sites that are characterized as having moderately high to high abundances. To elucidate driving factors of mussel Keywords: Rocky shores abundances in these regions, we investigated recruitment and growth rates of mussels in 1) northern and Recruitment rate southern California, two regions separated by ca. 900 km and exposed to vastly different oceanographic Growth rate processes and 2) within southern California at sites with moderately high mussel abundances and at sites Mytilus with low abundances. We found that recruitment and, to a degree, growth may be important factors driving Mussel bed variable abundances of mussels within southern California but could not explain patterns along the entire California coast. Recruitment and growth rates were low in northern California even though mussels were highly abundant. Conversely, recruitment and growth in southern California were signiﬁcantly higher than northern California and, within the region, were higher in sites characterized by moderately high abundances. Among regions, differences in recruitment and growth are likely driven by large scale oceanographic patterns such as upwelling affecting larval transport and temperature affecting growth. Within southern California, local oceanographic processes likely enhanced or inhibited recruitment or growth leading to differences in measures between closely located sites. Published by Elsevier B.V.

1. Introduction be linked to the frequency of upwelling and relaxation events leading to differing levels of larval supply (Roughgarden et al., 1988; Connolly Macroinvertebrate communities in rocky intertidal habitats are and Roughgarden, 1998). Furthermore, oceanographic conditions influenced by benthic processes, such as competition and predation, bringing phytoplankton nearshore can drive rocky intertidal commu- and physical disturbance, such as that from wave activity, which can nities towards those dominated by filter feeders as opposed to macro- drive patterns of abundances of adult populations (e.g. Connell, 1961; phyte dominated communities where plankton supply is low (Menge Paine, 1966; Dayton, 1971). Equally important are oceanographic et al., 1997). conditions that, for example, can carry larvae on- or offshore (e.g. Along the eastern north Pacific coast, the mid rocky intertidal Roughgarden et al., 1988) or supply coastal communities with zones on wave-exposed shorelines are dominated by mussels, mostly nutrients for primary productivity or food for benthic filter feeders Mytilus californianus Condrad (Ricketts et al., 1968). Mussels congre- (e.g. Menge et al., 1997, 1999, 2003; Blanchette et al., 2002, 2006). For gate in large clumps that can be several layers thick forming a mussel example, adult barnacle abundances differ greatly along the eastern bed that can provide space and shelter for a large number of associated North Pacific coast, with high barnacle cover in Oregon and low cover species. In addition, as filter feeders that consume large amounts of in the northern and central portions of California, that are suggested to plankton and detritus, they function as an energy link between pelagic and benthic systems providing secondary production for a wide number of predators. A survey of mussel abundances along three ⁎ Corresponding author. Current address: Department of Biological Science, regions of the California coast (southern, central, and northern) reveals California State University, Fullerton, P.O. Box 6850, Fullerton, CA 92834-6850, United States. high variability among regions (particularly between southern and E-mail address: [email protected] (J.R. Smith). northern California) as well as among sites within a region (Smith,

1385-1101/$ – see front matter. Published by Elsevier B.V. doi:10.1016/j.seares.2008.10.009 166 J.R. Smith et al. / Journal of Sea Research 61 (2009) 165–173

2005). In general, mussel abundances are relatively low throughout Recently, there have been a number of studies attempting to the Southern California Bight (SCB), including both the mainland and elucidate the importance of larger scale oceanographic conditions on offshore islands, and central California but are much more abundant in mussel distributions (Broitman et al., 2005; Phillips, 2005; Blanchette northern California (Monterey Bay and north). Despite this regional et al., 2006, 2007; Blanchette and Gaines, 2007). On Santa Cruz Island, trend, there are numerous locations in the SCB that are characterized one of the southern California offshore Channel Islands (see Fig. 1), with moderate to high mussel abundances. The driving forces behind the western side of the island experienced cold temperatures, a these patterns are unknown and likely attributed to multiple factors. higher frequency of upwelling, and low recruitment rates as com- Here, we explore patterns of recruitment and growth within and pared to opposite patterns on the eastern side (Broitman et al., 2005). between southern and northern California, two regions with differing Recruitment rates, abundances, and growth of mussels in this region oceanographic conditions, to elucidate whether these variables are were positively associated with sea surface temperatures. Food linked to adult mussel abundances. availability, as indicated by chl-a concentrations, were not related Mussel abundances can be driven by numerous biotic and abiotic (Blanchette et al., 2006). Additional studies have compared mussel factors on both local and large geographic scales. On a local scale, populations in the immediate area surrounding Point Conception, a mussels are affected, for example, by sea star predators that can biogeographic break separating colder central California waters from control abundances as well as the distribution of mussels into the low warmer southern California waters (see Fig. 1). Here, warmer southern intertidal zone (Paine, 1966, 1974). Desiccation and submergence time, California waters with higher mussel abundances were found to have or the amount of time available for feeding, also have been shown higher growth rates that were related to temperature and wave expo- be important driving forces in mussel abundances and distributions sure but, again, were not correlated with food availability (Phillips, (Dehnel, 1956; Harger, 1970; Behrens Yamada and Dunham, 1989; 2005; Blanchette et al., 2007). Abundances north and south of Point Harley and Helmuth, 2003). Conception were not driven by differential recruitment as recruitment Mesoscale (100s of km) oceanographic conditions are also an was low in the entire region (Blanchette and Gaines, 2007). important driving force for adult mussel populations. Supply of food Despite numerous reports on oceanographic conditions and their and mussel larvae varies greatly depending on numerous oceano- influence on mussel community dynamics, gaps in our knowledge still graphic patterns, most notably upwelling and relaxation events exist. Much of the previously published work has concentrated on (Farrell et al., 1991; Roughgarden et al., 1991; Miller and Emlet, 1997). areas immediately surrounding Point Conception in the northern Because meroplanktonic larvae and other planktonic organisms are portion of the SCB by Santa Barbara and central California. Little work carried by currents, recruitment and food supply patterns are heavily has been conducted in the other portions of southern California (i.e.. influenced by movement of coastal water masses on- or offshore Los Angeles and San Diego; see Fig. 1). In addition, few comparisons (Farrell et al., 1991; Roughgarden et al., 1991, 1994; Gaines and have been conducted on recruitment and growth between the SCB Bertness, 1992; Shanks et al., 2000; McCulloch and Shanks, 2003). and northern California. The purpose of this study was to compare During periods of upwelling, plankton travel with water masses recruitment and growth of mussels in two regions, southern and moving offshore and accumulate at offshore frontal boundaries where northern California, subjected to different oceanographic patterns and cold and saline upwelled water meets warmer and less saline water characterized by differing adult abundances. Recruitment and growth (Roughgarden et al., 1994). This convergence zone can move, of mussels were measured at several sites in southern and northern depending on the winds, and can transport larvae or planktonic food California to determine geographic differences between the two onshore during periods of relaxed upwelling (Farrell et al., 1991; regions and at sites within southern California with differing adult Roughgarden et al., 1991; Miller and Emlet, 1997). mussel characteristics to determine if there is a relationship with The supply of larvae can have important implications in rocky adult mussel populations. intertidal community structure (e.g. Underwood et al., 1983; Gaines and Roughgarden, 1985; Connolly and Roughgarden, 1998; Connolly 2. Methods et al., 2001). When larval supply is limited, the importance of benthic processes is much reduced and adult macroinvertebrate abundances 2.1. Site Selection are driven more by recruitment rates (Underwood et al., 1983; Gaines and Roughgarden, 1985; Ebert and Russell, 1988; Roughgarden et al., Nine sites were selected in two non-adjacent regions, northern and 1988; Farrell et al., 1991; Connolly et al., 2001). Furthermore, low southern California, separated by ca. 900 km of coastline (Fig. 1). The larval supply driven by coastal upwelling dynamics can influence SCB is characterized as a transition zone between temperate and community composition by enhancing conditions whereby macro- subtropical regimes with sea surface temperatures ranging yearly algae dominate space (Schiel, 2004). When larval supply is not limited, from ~11 to 23 °C. Upwelling events in the region are infrequent and benthic interactions, such as competition and predation, are more often only occur in short time periods during the spring season (Littler, intense (Gaines and Roughgarden, 1985; Connolly and Roughgarden, 1980; Hickey, 1993). Much of the southern California mainland coast- 1998; Connolly et al., 2001). line is protected from large swell events because of the orientation of Besides larval supply and recruitment, post-settlement processes the coast and the presence of the Channel Islands that act as a barrier to such as growth rates also can be important in structuring adult long-distance swell events. Northern California is subjected to much populations of macroinvertebrates (Gaines and Roughgarden, 1985; colder waters ranging yearly from ~8 to 17 °C. Upwelling in northern Bertness et al., 1991; Connolly and Roughgarden, 1998; Blanchette California is more intense and longer with few relaxation events et al., 2007). Variable growth rates may affect community structure (Bakun and Nelson, 1991). Locations along the northern California and population interactions (Bertness et al., 1991), and, in turn, coastline are also seasonally exposed to large swell events. adult populations through alterations of susceptibility to physical Of the nine sites selected, six sites were located in the SCB and stress (Vermeij, 1971), predation (Paine, 1976; Robles et al., 1990), and three sites in northern California. Six sites were chosen within competition (Buss, 1986) and availability of free space (Gaines and southern California, a region with variable mussel abundances, with Roughgarden,1985). In addition, growth rates impact the reproductive three locations considered to have moderate to high mussel potential of the population as reproductive output increases expo- abundances and thick beds and three with low abundances and thin nentially with size (Kautsky, 1982). Oceanographic regimes, mostly beds. In northern California, a region characterized by consistently temperature but also supply of food, can greatly influence growth high mussel abundances and very thick beds, only three locations rates along local (among sites) and larger geographic scales (among were chosen. The scale of mussel abundances (high to low) was based regions). on measures of mussel bed thickness at each of the locations. Bed J.R. Smith et al. / Journal of Sea Research 61 (2009) 165–173 167

Fig. 1. Map of nine sampled sites along the wave-exposed coast of California. Also indicated are the three regions of California: southern CA separated from central CA at Point Conception and northern CA separated from central CA at Monterey. thickness was measured at twenty random points in five 0.5×0.7 m regions or sites as mussel bed size depends on the slope and size of the quadrats randomly placed within the middle of established mussel intertidal zone which can be highly variable among locations and beds for a total of 100 points. At each of these points, a steel pin was between regions. Instead, measures of mussel abundances within pushed through the bed until it reached the understory rock and the established beds were used as considered by others (Blanchette and length measured. Mussel bed thickness was used as a proxy for mussel Gaines, 2007). The three SCB sites considered to have low mussel abundances as it was found to be steeply and positively related with abundances were characterized with thin, single layered beds mea- biomass (R2 =0.92, pb0.001) and adult density (R2 =0.54, pb0.001; suring 40.9±2.7 (mean±SE) mm deep while the three sites considered Smith, 2005). The areal extents of the mussel beds were not measured to have moderate/high mussel abundances were relatively thick and but are not likely good comparisons of mussel abundances across multi-layered reaching 95.4±10.7 mm in depth (site specific measures 168 J.R. Smith et al. / Journal of Sea Research 61 (2009) 165–173 in Table 1). The northern California sites were characterized by very growth, similar methods were used at all sites to ensure compar- thick mussel beds (145.5±10.9 mm; Table 1). ability. The entire length of the mussel was measured initially. An etch mark was then made near the posterior shell edge of each mussel, and 2.2. Recruitment the length from the etch mark to the posterior lip of the mussel was measured. Similar methods of marking mussels have been used in At each site, 6 or 7 recruitment collectors (Tuffy brand pot other growth studies (Seed, 1976; Behrens Yamada and Peters, 1988; scrubbers) were bolted to the rock within mussel beds and replaced Behrens Yamada and Dunham, 1989; McQuaid and Lindsay, 2000; every month for 1 year starting March 2003. Tuffies were placed in the Steffani and Branch, 2003; Blanchette et al., 2007). Every three to four middle of mussel beds to standardize effective tidal heights among months for 1 year, the etch mark to the lip was re-measured to sites, since mussel bed tidal height ranges may vary due to facing monitor growth and standardized to growth per month (30 days). slope, wave action, and other oceanographic or geologic factors. Tuffy Because a portion of the mussels or tags were periodically lost, new scrubbers have been commonly used for mussel recruitment mea- mussels were tagged and measured approximately every three to four sures (e.g. Menge, 1992; Phillips and Gaines, 2002) as they simulate months during resampling periods in order to maintain a sufficient the physical structure of filamentous algae and byssal threads in sample size. Despite loss of tags, data were not compromised as we which mussel larvae normally settle (Petersen, 1984). Collected Tuffies examined growth rates for the site population for each season; we did were returned to the lab and frozen until further analysis. not attempt to measure growth for the populations at each site over a Recruitment collectors were processed by thawing the Tuffy, year period. Monthly mussel growth was calculated for four seasons rinsing with fresh water, and collecting all solid materials in a 250 µm throughout the year-long study. Although we attempted to use the sieve. Recruits were counted under a dissecting microscope. In many same range of initial sizes of mussels, the size frequency of tagged cases, only 3 or 4 collectors were processed per month, as variation individuals varied at sites depending on the population size frequency. within a month at a site was small. In a few cases, collectors were lost, In addition, the size frequency of tagged mussels also varied seas- possibly due to wave activity or human intervention, reducing the onally due to lost tags and several remarking sampling efforts. For sample size to two collectors at sites in certain months. The mean presentation purposes, all data are included in the figures. However, number of recruits per collector per month was calculated for each to account for variability in the number of replicates in the small site. Although Mytilus recruits were not identified to species, obser- and large size classes, we truncated our data to include only those vations of newly recruited mussels into open patches and subsequent individuals with an initial length between 40 and 60 mm. aging to juvenile and adult mussels suggested that only Mytilus californianus were recruiting to the sites. The bay mussel Mytilus 2.4. Analysis galloprovincialis Lamarck, a less common species on the open coast, has been observed to exhibit episodic recruitment to the wave- Recruitment and growth data were analyzed using the Minitab exposed rocky intertidal zone (Smith per. obs.) but are easily distin- statistical program (version 13.0). Data were tested for normality and guishable as juveniles. During this study, M. galloprovincialis were not homogeneity of variance and transformed when necessary. To test for seen in mussel cohorts observed throughout the year-long experiment spatial differences in recruitment, a Nested Two Factor ANOVA was and were rare in harvested samples of already established adult performed with region (southern v northern California) and month as mussel populations (Smith, 2005). Furthermore, previous studies on fixed factors and sites nested within regions. The mean number of mussel recruitment have found that more than 90% of collected mussel recruits collector− 1 month− 1 (log transformed) was calculated recruits are Mytilus californianus (see Blanchette and Gaines, 2007). for twelve months at all sites in southern California and compared with sites in northern California. To determine if recruitment varied 2.3. Growth among beds in southern California with differing adult mussel populations, we calculated the mean number of mussel recruits collector− 1 At each site, 80 mussels of a range of sizes (25–80 mm, but mostly month− 1 for twelve months at sites with mussel populations within 40–60 mm range) were haphazardly chosen and tagged in characterized by thick beds and compared them with recruitment at March of 2003. Tagged mussels were located in the middle of mussel sites with thin beds. Log transformed data were analyzed using a beds to standardize effective tidal heights. Numbered wire tags were Nested Two Factor ANOVA with bed thickness type (thick v thin) and superglued to the surface of mussels and each mussel mapped using a month as factors and sites nested within bed thickness type. grid system. For ease of sampling and to limit damage of the mussel Growth data for each individual were converted to growth (mm) bed through manual movement of mussels and weakening of their per 30 day month (mm) and tested for normality and homogeneity of attachment strengths, only mussels on the upper surface of the bed variance. To test for regional differences in growth, a Nested Two Factor were marked. Although measuring growth of surface mussels may ANCOVA was used on untransformed data with region and season as bias results by monitoring mussels that likely exhibit the highest fixed factors, sites nested within regions, and initial size as a co-variate. To determine if growth varied among locations in southern California Table 1 with differing adult populations, untransformed growth data were Site name, abbreviation, county, and location (latitude and longitude) analyzed using a Nested Two Factor ANCOVA with bed thickness type Site Site code County Location Bed thickness and season as fixed factors, sites nested within bed thickness type, and (mm) initial size as a covariate. In order to present the large data set in a clear Southern California manner, several graphs were constructed indicating the regression line Ocean Beach OCB San Diego 32° 44′ 38″ 117° 15′ 19″ 35.8 (4.0) of growth per month plotted against initial size. Three graphs were Carlsbad CBD San Diego 33° 06′ 45″ 117° 20′ 41″ 88.0 (8.6) Treasure Island TRE Orange 33° 30′ 48″ 117° 45′ 33″ 42.2 (3.9) constructed showing: 1) each site individually across all seasons, Crystal Cove CRC Orange 33° 34′ 13″ 117° 50′ 15″ 106.8 (8.2) 2) combined southern and northern California sites for each of the four Point Fermin PTF Los Angeles 33° 42′ 26″ 118° 17′ 09″ 44.8 (1.8) seasons, and 3) combined locations within southern California with ′ ″ ′ ″ Tuna Canyon TUN Los Angeles 34° 02 20 118° 41 17 91.4 (15.5) thick beds/high mussel abundances and locations with thin beds/low

Northern California abundances for each of the four seasons. Bolinas BOL Marin 37° 54′ 13″ 122° 43′ 34″ 125.8 (7.4) We attempted to construct von Bertalanffy growth curves and Bodega Head BOD Sonoma 38° 18′ 58″ 123° 04′ 19″ 163.5 (13.9) compare these slopes to determine differences among sites. However, Sea Ranch SEA Sonoma 38° 43′ 48″ 123° 29′ 18″ 147.3 (12.2) growth at some sites was practically absent and, with a small degree Also reported is mean site bed thickness (±SE) for all nine sites (Smith, 2005). of measuring error, some individuals exhibited negative growth. In J.R. Smith et al. / Journal of Sea Research 61 (2009) 165–173 169 addition, because growth was extremely low, faster rates of growth in Table 2 small mussels as compared to large mussels at some sites could not be Summary of statistical results for Two Factor ANOVAs on recruitment and Two Factor ANCOVA on growth data detected. Due to these issues, growth curves could not be satisfactorily constructed. Data Factor df MS Fpvalue Recruitment Region 1 26.10 59.7 b0.001 3. Results Month 1 0.361 1.3 0.250 Region×Month 1 1.68 6.2 0.013 Site (region) 7 16.20 59.7 b0.001 3.1. Recruitment Thickness 1 7.46 34.7 b0.001 The mean number of recruits per artificial collector over the year Month 1 0.38 1.8 0.183 sampling period was highest at Carlsbad and Tuna Canyon in the SCB Thickness×Month 1 0.72 3.3 0.069 Site (thickness) 4 9.68 45.0 b0.001 and was lowest at Bolinas and Sea Ranch in northern California (Fig. 2). Growth Initial size (covariate) 1 4.99 5.43 0.020 The largest number of recruits found in one collector throughout the Region 1 11.12 12.2 0.001 study was ~1550 recruits at Carlsbad in August. Sites in northern Season 1 4.76 5.2 0.023 California had consistently low recruitment while southern California Region×Season 1 10.19 11.1 0.001 sites were highly variable. Averaging sites within a region revealed Site (region) 7 11.59 12.6 0.001 very low monthly recruitment rates in northern California while Initial size (covariate) 1 7.87 5.0 0.015 recruitment rates in the SCB were an order of magnitude higher Thickness 1 2.39 1.8 0.178 (Fig. 2). A Nested Two Factor ANOVA revealed significant differences Season 1 0.82 0.6 0.430 between regions and among sites nested in regions while a temporal Thickness×Season 1 0.76 0.6 0.446 Site (thickness) 4 6.88 5.3 b0.001 trend was not detected. A significant interaction between region and month was found (Table 2) with weak patterns of temporal differ- Reported are degrees of freedom (df), mean squares (MS), F stat, and p values for each of fi ences in some locations in the SCB, mostly driven by high rates of the analyzed factors. Signi cant p-values are indicated in bold. recruitment at Carlsbad in late summer/early fall. Within the SCB, two of the three sites with thick beds/high adult abundances had much higher recruitment rates than the three sites vidual (Fig. 3a). Overall, mussels at Tuna Canyon grew the fastest; the with thin beds/low adult abundances (Fig. 2). Here, only 9.4±1.3 exception was small mussels at Point Fermin, which grew slightly (mean±SE) recruits per month per collector were counted in thin beds faster but with the rate of growth slowing markedly with larger as opposed to 79.1±13.7 recruits per month per collector in thick beds. individuals. The lowest growth occurred at the three northern In southern California, recruitment rates were significantly higher in California sites. Most sites in southern California exhibited slightly the sites with thick beds than those sites with thin beds with negative growth slopes with increasing size except Point Fermin, significant differences also found among sites nested within thick or which exhibited a much steeper negative slope. In northern California, thin beds (Nested Two-Factor ANOVA, Table 2); temporal differences slopes varied among sites but were relatively flat due to low growth and an interaction effect were not detected. overall. Between regions, growth was significantly higher in the SCB than in northern California with significant differences among sites 3.2. Growth nested within regions (Fig. 3a,b; Nested Two Factor ANCOVA, Table 2). In addition, growth rates differed significantly among seasons Growth rates were low and ranged from almost no growth to (Table 2) with relatively high growth in summer and spring for both ~3 mm month− 1 depending on the site and initial size of the indi- regions and lowest growth in winter (Fig. 3b). In fall, growth rates

Fig. 2. Mean number of mussel recruits per collector per month (±SE) for six southern California sites and three northern California sites. In southern California, sites with thick mussel beds (high abundance) are noted by black bars while gray bars note sites with thin beds. All sites within northern California had thick beds. Mean recruitment rates (±SE) are noted for the southern and northern California regions and for thick and thin beds within southern California. 170 J.R. Smith et al. / Journal of Sea Research 61 (2009) 165–173

Fig. 3. Slope of growth of marked mussels (mm per month) versus initial size (mm) for a) all nine sites sampled combining all seasons, b) southern California sites combined and northern California sites combined during the four sampled seasons (F03=Fall 2003; SU03=Summer 2003; SP03=Spring 2003; and W04=Winter 2004), and c) southern California sites with locations characterized by thick mussel beds (=high mussel abundance) combined and thin mussel beds (=low mussel abundance) combined during the four sampled seasons. Site abbreviations are located in Table 1. Length of slopes are artiﬁcially extended or cut-off at 80 mm. The shaded region indicates the size class that was used for statistical analyses (see Methods).

across all sizes were higher than any other season in southern 4. Discussion California. In northern California, there was a positive slope causing a significant interaction between region and season (Table 2). Recruitment and growth were important factors affecting the Within the SCB, overall growth was generally higher in the three distribution of mussels within the southern California Bight (SCB) but locations characterized with thick beds than locations with thin beds could not explain patterns along the entire California coast. Higher (Fig. 3a,c). Sites nested within bed thickness were found to be recruitment and growth in mussel populations in the SCB character- significantly variable but no difference was found between the thin ized by low to moderately high adult abundances were contrasted and thick beds (Nested Two Factor ANCOVA, Table 2). In fall, growth with low recruitment and growth in northern California, a region ranked the highest for both bed types with a pattern of small to with markedly higher adult abundances. Within the SCB, recruitment medium sized mussels growing faster in thin beds than thick beds and growth were related to the level of adult abundances as locations (Fig. 3c). In thick beds, there were little differences in growth or slopes with thick beds (higher adult mussel abundances) had higher among seasons. In thin beds, however, growth rates and growth slopes recruitment and growth rates than locations with thin beds (lower varied with season: in summer and winter, growth slopes were flat or abundances). Geographic trends in recruitment and growth across a slightly positive while slopes in fall and spring were negative. Growth large geographic scale that differ oceanographically suggest that among seasons, however, was not found to differ significantly nor was different processes affected mussel populations within the two an interaction found between bed type and season (Table 2). regions. J.R. Smith et al. / Journal of Sea Research 61 (2009) 165–173 171

4.1. Recruitment ment rates differed greatly at sites in close proximity (i.e.., Tuna Canyon and Point Fermin) with no obvious geomorphological differ- Larval transport and recruitment are known to be heavily ences that could affect oceanographic patterns. However, it is influenced by oceanographic processes. Coastal circulation promotes interesting to note that Carlsbad, the site with highest recruitment, transport of larvae to the shore in some areas, such as Oregon, while is located near the mouth of Agua Hedionda Lagoon. Here, local in other areas, such as northern and central California, frequent oceanography may be influenced by the lagoon and may result in upwelling events transport larvae offshore (Roughgarden et al., 1988, larval transport onshore. Studies investigating river plume and Connolly and Roughgarden, 1998). Recruitment at sites in northern estuarine front dynamics suggest that buoyant coastal discharges California was consistent with patterns produced by strong upwelling may induce coastal currents locally, causing a frontal circulation at the and offshore transport of larvae. Results suggest, in accordance with mouth that acts as a barrier to larvae dispersal (Kingsford and Suther, other studies (e.g. Broitman et al., 2005, 2008), that mussels are 1994; Vargas et al., 2006). Here, accumulation of larvae at the front potentially limited where upwelling is frequent. In the SCB, however, edge may facilitate transport to some locations nearby (Eggleston upwelling is generally weak and sporadic (Hickey, 1993). The et al., 1998; Vargas et al., 2006) as the plume circles back around near oceanographic regime in the SCB may be facilitating larval transport the coastline. Although flow out of Agua Hedionda is likely low, a front and higher recruitment to rocky intertidal habitats in the region. Ebert may occur near the mouth where mussel larvae may accumulate and et al. (1994) reported higher recruitment of urchins in southern then be transported back to shore during relaxation of estuarine California compared to northern California and suggested that the driven fronts (Eggleston et al., 1998) or when strong tidal movements pattern was likely due to greater retention of water in the SCB. move the front shoreward. Recruitment rates of Mytilus at many of our southern California It is clear from other work (Broitman et al., 2008) that there is some locations were similarly low to other locations in the region level of year-to-year variation in recruitment rates possibly due to (Blanchette and Gaines, 2007; Broitman et al., 2008). These locations, temporal variation in upwelling frequency and longevity. Our study although with higher recruitment rates than northern California, were monitored recruitment over a year period and thus did not detect several magnitudes lower than observed in Oregon, a region with longer term temporal change. Nonetheless, the regional patterns we intermittent upwelling (Broitman et al., 2008). However, contrasting detected are unlikely to change over time as geographic recruitment other SCB recruitment studies, we found two locations in the central patterns appear consistent over multiple years (Broitman et al., 2008). portion of the bight where recruitment was relatively high. On Here, above and below normal levels of recruitment during certain occasion, recruitment rates at Carlsbad were extremely high with years of recruitment monitoring along the eastern north Pacific coast levels similar to that of Oregon. This high variability in the region appeared consistent among regions. denotes the need for long term recruitment monitoring studies to include more location into the southern and central portions of the 4.2. Growth SCB. The factors leading to high recruitment at some sites within the Growth of mussels, like recruitment, showed geographical varia- SCB need to be further investigated. It is unlikely that the adult pop- tions with southern California exhibiting higher growth than northern ulation is regulating the number of recruits through local recruitment California. Geographical differences in growth rates likely reflect dif- from the resident population, as Mytilus californianus has exhibited no ferences in temperature between the two regions. Phillips (2005) and difference in large-scale proportions of genetic types, suggesting that Blanchette et al. (2007) suggested that observed differences in growth gene flow occurs along the coastline and that mussel larvae disperse between sites north and south of Point Conception were likely long distances (Engel, 2004). Alternatively, very nearshore oceano- attributable to temperature differences. Within southern California, graphic processes at each of the sites may explain differences in growth rates of mussels and barnacles were found to be positively recruitment rates. Several processes on a local level may affect larval correlated with SST (Blanchette et al., 2006) when comparing growth supply including internal waves, surface slicks and foam lines, at sites on a southern California offshore Channel Island subjected to a and Langmuir flow (Shanks, 1983, 1995; Kingsford and Choat, 1986; persistent thermal gradient on opposite sides of the island. Mussels Shanks and Wright, 1987; Kingsford, 1990; Kingsford et al., 1991; are known to grow rapidly in temperature between 15 and 19 °C, with McCulloch and Shanks, 2003; Shanks et al., 2003). For example, at decreases in growth observed in temperatures above and below that sites with low recruitment, local currents may transport incoming range (Coe and Fox, 1942, 1944). At the southern California sites, mean larvae seaward or topographically generated fronts may act as a annual temperatures (1995–2003; Advanced Very High Resolution barrier to larvae reaching the shore (McCulloch and Shanks, 2003). Radiometer) among sites ranged from 16 to 17 °C, within the range of Similarly, local currents or topography may facilitate high recruitment highest mussel growth, while yearly mean temperatures at our by transporting larvae inshore. Several studies (Shanks, 1983, 1986; northern sites were approximately 12 °C, well below the range of Kingsford and Choat, 1986; Kingsford et al., 1991) have reported optimal growth. that some larvae of coastal invertebrates and fishes are transported Food availability can also be a factor influencing mussel growth as shoreward in surface slicks generated over tidally forced internal filter feeders are known to exhibit higher growth in areas with higher waves. Some meroplanktonic larvae can also behaviorally utilize food availability (e.g. Duggins et al., 1989; Bertness et al., 1991; vertically sheared flows to aid shoreward progression (Garland et al., Dahlhoff and Menge, 1996; Menge et al., 1997; Sanford and Menge, 2002). For example, offshore larvae from benthic populations can be 2001). However, recent work has suggested that other factors may be carried toward the coast during periods of upwelling as bottom water determining growth rates, either separately or in conjunction with flows towards the shoreline (Garland et al., 2002). Other invertebrate productivity (Sanford and Menge, 2001; Phillips, 2005; Blanchette larvae may be retained between the shore and an upwelling front due et al., 2006). Numerous studies have reported that growth of mussels to diel vertical migrations (Poulin et al., 2002). Understanding local and other filter feeders north and south of Point Conception was variations in recruitment of invertebrates with broadly dispersing not explained by food availability or food quality (Phillips, 2005; larvae and the processes affecting these variations can aid in under- Blanchette et al., 2006, 2007). They suggested that temperature likely standing how to manage and conserve at-risk populations. This is played a more significant role in determining growth. Measures of especially important for mussels in southern California where popu- food availability were beyond the scope of this study thus we cannot lations have declined over the past few decades (Smith et al., 2006). expand on the effects on growth at our sites. Without knowledge of specific local oceanography at our sites, it Unlike regional differences, variation in growth in southern is difficult to ascertain reason for differing recruitment rates. Recruit- California could not be attributed to temperature, since all sites 172 J.R. Smith et al. / Journal of Sea Research 61 (2009) 165–173 within the SCB fell within the temperature range of highest growth Within southern California, and sometimes in close proximity (Coe and Fox, 1942, 1944). Furthermore, sites with low growth were in (b50 km), recruitment and growth can be highly variable. Under- close proximity (b50 km) to sites with high growth and thus had very standing local physical mechanisms underlying larval transport and similar seawater temperatures. Although Blanchette et al. (2006) growth will lead to a better understanding of adult populations and attributed differences in growth between locations in close proximity potential management of coastal species, especially those important within southern California to temperature, they conducted work on an to fisheries and local economy. offshore island subjected to quite different thermal regimes on opposite sides of the island. Acknowledgements Alternative to temperature causing variability in growth rates within southern California, potential factors such as food availability We are thankful to the Environmental Protection Agency, the and wave activity may be important local factors/drivers. First, Minerals Management Service through the Coastal Marine Institute at although cholorophyll a, an indicator of food availability, was con- the University of California, Santa Barbara, and the UCLA Ecology and sistently low throughout the SCB using satellite data from large areas Evolutionary Biology Department for their assistance in funding this (40×50 km — meridional×zonal; Smith, 2005 also supported by project. We also thank several assistants in the processing of recruit- nearshore measurements by Blanchette et al., 2007), local scale ment sampling including David Lin, Koosha Aghajani, Chia Lin, dynamics may result in increased food availability at certain locations Danielle Whitehead, and Vanessa Gonzalez. We are grateful to several that may not be detectable in larger scale measures of productivity. sources for permission and access to sites including Peter Connors and For example, terrestrial runoff discharging into a particular site may the UC Davis Bodega Marine Lab; Linda Weinstein and the Sea Ranch result in elevated nutrient levels and thus increased productivity. Association; Pamela Higgins and the Carlsbad State Beach; and David Although runoff was not prominent at most sites, Carlsbad, the site Pryor and the Crystal Cove State Beach. We also thank Carol Blanchette with the highest growth, is located near the Agua Hedionda Lagoon for the suggestions and input into the manuscript. outlet that may serve as a source of nutrients and/or food. Wave activity may also play a role in determining growth at these sites and References has been correlated with higher growth rates at other SCB locations (Blanchette et al., 2007). Although not directly measured, repeated Bakun, A., Nelson, C.S., 1991. The seasonal cycle of wind-stress curl in subtropical – observations of wave activity at sampled sites suggest that Carlsbad is Eastern boundary current regions. J. Phys. Oceanogr. 21, 1815 1834. Behrens Yamada, S., Peters, E.E., 1988. Harvest management and the growth and condi- the most wave-exposed followed by Treasure Island and Tuna Canyon; tion of submarket-size sea mussels, Mytilus californianus. Aquaculture 74, 293–299. Carlsbad and Tuna Canyon are two of three sites with high mussel Behrens Yamada, S., Dunham, J.B., 1989. Mytilus californianus, a new aquaculture – abundances and high growth. Finally, local currents may bring off- species? Aquaculture 81, 275 284. Bertness, M.D., Gaines, S., Bermudez, D., Sanford, E., 1991. 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